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_ VOL. 21 1981

MALACOLOGIA

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

Internationale Malakologische Zeitschrift

Publication date
Vol. 20, No. 2—17 June 1981

MALACOLOGIA, VOL. 21
CONTENTS

SECOND INTERNATIONAL SYMPOSIUM ON EVOLUTION
AND ADAPTIVE RADIATION OF MOLLUSCA
SPONSORED BY
UNITAS MALACOLOGICA
SEVENTH INTERNATIONAL MALACOLOGICAL CONGRESS
PERPIGNAN, FRANCE. 31 August-7 September 1980

P. BOUCHET

Evolution of larval development in eastern Atlantic Terebridae

(Gastropoda), Neogenetto Recent acc. do sauna ans. 363
A. J. CAIN

Variation in shell shape and size of helicid snails in relation to

other pulmonates in faunas of the Palaearctic region ...................... 149
P. CALOW

Adaptational aspects of growth and reproduction in Lymnaea
peregra (Gastropoda: Pulmonata) from exposed and shel-

CELE a dl e A ae en A 5
G. M. DAVIS

ИЕ О КО ne RUSSES PAR ANRT, en CA ее 1
С. М. DAVIS

Different modes of evolution and adaptive radiation in the

Pomatiopsidae (Prosobranchia: Mesogastropoda) ......................... 209
V. FRETTER, A. GRAHAM and J. H. McLEAN

The anatomy of the Galapagos rift limpet, Neomphalus fretterae ........... 337
W. HAAS |

Evolution of calcareous hardparts in primitive molluscs .................... 403
K. E. HOAGLAND and R. D. TURNER

Evolution and adaptive radiation of shipworms (Bivalvia, Teredinidae) ....... Wala

R. S. HOUBRICK
Anatomy, biology and systematics of Campanile symbolicum with
reference to adaptive radiation of the Cerithiacea (Gastropoda:

FALSE UC Mea) N RENTE ARE Wie States SO ae eR RR ER 263
J. H. McLEAN

The Galapagos rift limpet Neomphalus: relevance to under-

standing the evolution of a major Paleozoic-Mesozoic radiation ............ 291
B. MORTON

see ee ee SIN ets С ее ия 35
W. NARCHI

Aspects of the adaptive morphology of Mesodesma mactroides

(EAN A o II A A: cages wee ded es 95
P. G. OLIVER

The functional morphology and evolution of Recent Limopsidae

NEE fe NP A APR PR A 61

L. v. SALVINI-PLAWEN
The molluscan digestive system in evolution .............................. 371

$. TILLIER

MALACOLOGIA

CONTENTS (cont.)

Clines, convergence and character displacement in New Caledonian
diplommatinids (land) prosebranehs) 22°... 2. SE CE ne

E. R. TRUEMAN and H. B. AKBERALI
Responses of an estuarine bivalve, Scrobicularia plana (Tellinacea)

tO" SMCSS Hee oe is.

C. M. YONGE

On adaptive radiation in the Pectinacea with a description of Hemi-

pecten forbesianus

AWARDS FOR STUDY АТ
The Academy of Natural Sciences of Philadelphia

The Academy of Natural Sciences of Philadelphia, through its Jessup and McHenry
funds, makes available each year a limited number of awards to support students
pursuing natural history studies at the Academy. These awards are primarily intended
to assist predoctoral and immediate postdoctoral students. Awards usually include a
stipend to help defray living expenses, and support for travel to and from the
Academy. Application deadlines are 1 April and 1 October each year. Further infor-
mation may be obtained by writing to: Chairman, Jessup-McHenry Award Committee,
Academy of Natural Sciences of Philadelphia, 19th and the Parkway, Philadelphia,
Pennsylvania 19103, U.S.A.

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VOL. 21 NO. 1-2 MUS comas 1981

HARVARD

UNIVERSITy

MALACOLOGIA

SEVENTH INTERNATIONAL MALACOLOGICAL CONGRESS
SYMPOSIUM PROCEEDINGS
Second International Symposium on Evolution
and Adaptive Radiation of Mollusca
5-6 September 1980, Perpignan, France

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

y Internationale Malakologische Zeitschrift

MALACOLOGIA
Editors-in-Chief:
GEORGE M. DAVIS ROBERT ROBERTSON

Editorial and Subscription Offices:

Department of Malacology
The Academy of Natural Sciences of Philadelphia
Nineteenth Street and the Parkway
Philadelphia, Pennsylvania 19103, U.S.A.

Associate Editors: Editorial Assistants:
JOHN B. BURCH MARY DUNN
University of Michigan, Ann Arbor GRETCHEN R. EICHHOLTZ
CHAMBERLIN

ANNE GISMANN
Maadi, A. R. Egypt

MALACOLOGIA is published by the INSTITUTE OF MALACOLOGY (2415 South Circle Drive,
Ann Arbor, Michigan 48103, U.S.A.), the Sponsor Members of which (also serving as editors)
are:

J FRANCES ALLEN, Emerita OLIVER E. PAGET
Environmental Protection Agency Naturhistorisches Museum, Wien, Austria

Washington, D.C.
ROBERT ROBERTSON
CHRISTOPHER J. BAYNE, President

Oregon State University, Corvallis CLYDE F. E. ROPER
Smithsonian Institution
ELMER G. BERRY, Emeritus Washington, D.C.

Germantown, Maryland W. D. RUSSELL-HUNTER, Vice-President

KENNETH J. BOSS Syracuse University, New York
Museum of Comparative Zodlogy
Cambridge, Massachusetts NORMAN F. ЗОНЕ |
United States Geological Survey
JOHN B. BURCH Washington, D.C.
MELBOURNE R. CARRIKER RUTH D. TURNER, Alternate
University of Delaware, Lewes Museum of Comparative Zoölogy
Cambridge, Massachusetts
GEORGE M. DAVIS, Executive
Secretary-Treasurer SHI-KUEI WU, President-Elect
University of Colorado Museum, Boulder
PETER JUNG

Naturhistorisches Museum, Basel, Switzerland

Institute meetings are held the first Friday in December each year at a convenient place. For
information, address the President.

1981

EDITORIAL BOARD

J. A. ALLEN

Marine Biological Station,
Millport, United Kingdom
E. E. BINDER

Muséum d'Histoire Naturelle
Genève, Switzerland

A. J. CAIN

University of Liverpool
United Kingdom

P. CALOW

University of Glasgow
United Kingdom

А. Н. CLARKE, yr.
Mattapoisett, Mass., U.S.A.
B. C. CLARKE

University of Nottingham
United Kingdom

E. S. DEMIAN

Ain Shams University
Cairo, A. R. Egypt

C. J. DUNCAN
University of Liverpool
United Kingdom

Z. A. FILATOVA
Institute of Oceanology
Moscow, U.S.S.R.

E. FISCHER-PIETTE
Muséum National d'Histoire Naturelle
Paris, France

V. FRETTER
University of Reading
United Kingdom

E. GITTENBERGER
Rijksmuseum van Natuurlijke Historie
Leiden, Netherlands

A. N. GOLIKOV
Zoological Institute
Leningrad, U.S.S.R.

S. J. GOULD

Harvard University
Cambridge, Mass., U.S.A.
A. V. GROSSU
Universitatea Bucuresti
Romania

T. HABE

Tokai University
Shimizu, Japan

A. D. HARRISON
University of Waterloo
Ontario, Canada

K. HATAI

Tohoku University
Sendai, Japan

B. HUBENDICK
Naturhistoriska Museet
Goteborg, Sweden

S. HUNT

University of Lancaster
United Kingdom

A. M. KEEN

Stanford University
California, U.S.A.

R. N. KILBURN

Natal Museum

Pietermaritzburg, South Africa

М. А. KLAPPENBACH

Museo Nacional de Historia Natural
Montevideo, Uruguay

J. KNUDSEN
Zoologisk Institut & Museum
Kobenhavn, Denmark

A. J. KOHN

University of Washington
Seattle, U.S.A.

Y. KONDO

Bernice P. Bishop Museum
Honolulu, Hawaii, U.S.A.

J. LEVER

Amsterdam, Netherlands

A. LUCAS
Faculté des Sciences
Brest, France

N. MACAROVICI
Universitatea “Al. I. Cuza”
lasi, Romania

C. MEIER-BROOK
Tropenmedizinisches Institut

Tübingen, Germany (Federal Republic)

H. K. MIENIS
Hebrew University of Jerusalem
Israel

J. E. MORTON
The University
Auckland, New Zealand

В. NATARAJAN
Marine Biological Station
Porto Novo, India

J. OKLAND
University of Oslo
Norway

T. OKUTANI
National Science Museum
Tokyo, Japan

W. L. PARAENSE
Universidade de Brasilia
Brazil

J. J. PARODIZ
Carnegie Museum
Pittsburgh, U.S.A.

W. F. PONDER
Australian Museum
Sydney

A. W. B. POWELL
Auckland Institute & Museum
New Zealand

R. D. PURCHON
Chelsea College of Science & Technology
London, United Kingdom

O. RAVERA
Euratom
Ispra, Italy

N. W. RUNHAM
University College of North Wales
Bangor, United Kingdom

S. G. SEGERSTRALE
Institute of Marine Research
Helsinki, Finland

G. A. SOLEM
Field Museum of Natural History
Chicago, U.S.A.

F. STARMUHLNER
Zoologisches Institut der Universitat
Wien, Austria

У. |. STAROBOGATOV
Zoological Institute
Leningrad, U.S.S.R.

W. STREIFF
Université de Caen
France

J. STUARDO
Universidad de Chile,
Valparaiso

T. E. THOMPSON
University of Bristol
United Kingdom

Е. TOFFOLER ©
Societa Malacologica Italiana
Milano

W. $. $. VAN BENTHEM JUTTING
Domburg, Netherlands

J. A. VAN EEDEN
Potchefstroom University
South Africa

J.-J. VAN MOL
Université Libre de Bruxelles
Belgium

N.H. VERDONK
Rijksuniversiteit
Utrecht, Netherlands

B. R. WILSON
National Museum of Victoria
Melbourne, Australia

С. М. YONGE
Edinburgh, United Kingdom

H. ZEISSLER

Leipzig, Germany (Democratic Republic)

A. ZILCH

Natur-Museum und Forschungs-Institut

Senckenberg

Frankfurt-am-Main, Germany (Federal

Republic)

SECOND INTERNATIONAL SYMPOSIUM ON EVOLUTION
AND ADAPTIVE RADIATION OF MOLLUSCA

SPONSORED BY
UNITAS MALACOLOGICA

Seventh International Malacological Congress
Perpignan, France
31 August-7 September 1980

JEAN-M. GAILLARD, PRESIDENT
Museum National d’Histoire Naturelle
Laboratoire de Biologie des Invertébrés Marins et Malacologie
55, rue de Buffon
75005 Paris, France

ORGANIZED BY

GEORGE M. DAVIS
Academy of Natural Sciences of Philadelphia
Nineteenth and the Parkway
Philadelphia, Pennsylvania, U.S.A.

CO-CHAIRMEN
Professeur MAXIME LAMOTTE Dr. CLAUS MEIER-BROOK
Laboratoire de Zoologie Tropenmedizinisches Institut der Universitat
Ecole Normale Supérieure D74 Tübingen
46 Rue d’Ulm Wilhelmstrasse 27

75005 Paris, France Federal Republic of Germany

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MALACOLOGIA, 1981, 21(1-2): 14

INTRODUCTION TO THE SECOND INTERNATIONAL SYMPOSIUM ON
EVOLUTION AND ADAPTIVE RADIATION OF MOLLUSCA

George M. Davis!

Academy of Natural Sciences, Nineteenth and the Parkway,
Philadelphia, Pennsylvania, U.S.A.

The Second International Symposium on
Evolution and Adaptive Radiation of Mollusca
was held in Perpignan, France, on the fifth
and sixth of September, 1980. This Symposi-
um was part of the Seventh International
Malacological Congress sponsored by Unitas
Malacologica.

As with the first symposium, the organizers
of the second symposium felt that a better
understanding of the relationships among
organisms could be obtained by studies
based on modern evolutionary biological
principles rather than solely by standard sys-
tematic practices. By standard practices, |
mean the systematic study of organisms in
order to assess relationships (or affinities,
Cain & Harrison, 1958) solely on the basis of
shared or different character states and to
erect, by whatever methods, an hierarchical
classification on the basis of the assessment.

Much more is to be gained if one considers
the evolutionary relationships among organ-
isms with particular emphasis on the adapta-
tion of organisms to their environments. Still
more is gained if one considers both historical
and ecological impacts on populations in
addition to the characters that allow one to
score similarities or differences among taxa. |
emphasize these aspects because one finds
very few papers that give us an objective ac-
count of the evolution and adaptive radiation
of any group of Mollusca.

What is meant by adaptive radiation?
Osborn (1918) created the term and dis-
cussed the concept at length. The concepts
involved in adaptive radiation and adaptive
zones were used and considerably expanded
by Simpson (1944, 1953, 1960), Wright
(1940), Huxley (1954), and many others to
explain the radiation of taxa they observed
where species were variously adapted to dif-
ferent niche dimensions but all had certain
morphological features in common. They de-

veloped the concept that a new radiation
might occur when a novel, genetically con-
trolled innovation is selected for by a shift in
environmental pressures. With selection for
this innovation, there is entrance into a new
adaptive zone and with it, the possibility for
speciation. With the invasion of new ecologi-
cal space such as terrestrial environments fol-
lowing the first vertebrate incursions, it was
argued that innovations would be selected in
small, peripherally isolated populations. Each
species in the new radiation has the morpho-
logical or physiological innovation but differs
from other species in character states reflect-
ing adaptations to different niche variables.
The historical element seen in the radiation is
the commonality of the innovative feature
marking entrance to the new adaptive zone.
As argued by Cain (1964) this historical ele-
ment is seen as a common feature because it
is adaptive, not because it is historical and
thus passively carried along.

One sees in the literature a broad, general-
ized concept of adaptive radiation (Simpson,
1953; Stanley, 1979). One speaks of the
mammalian radiation or the reptilian radiation.
There are, however, two different levels of
adaptive radiation that should be considered
in the study of macroevolution. One level |
have called macroradiation (Davis, this sym-
posium), which encompasses higher taxa,
such as the Mammalia, in which there are
several clades, which are genera, subfami-
lies, or yet higher taxa. The other level is a
subset of macroradiation and consists of a
single genus. This subset | call a first order
radiation. We see from an evolutionary bio-
logical viewpoint and from the discussion
above that a genus is not an arbitrary group-
ing of species. While it may be difficult, if not
impossible to delineate the whole phylogeny
of a macroradiation, it may be more possible
to work out the details of many first order radi-

1Supported, in part, by National Institutes of Health Grant TMP #11373.

(1)

2 DAVIS

ations. In this regard, it is not surprising to see
the intensive work now being done with what
have been considered species-rich genera
such as the land snail genera Partula (Murray
& Clarke, 1966, 1968), Cerion (reviewed by
Woodruff, 1978) and the marine snail genus
Patella (Branch, 1971, 1974a,b, 1975a,b,
1976), to mention only three.

Establishing a credible account of the evo-
lution of any group is not an easy task, and
may be impossible in many, if not most cases.
Cain & Harrison (1960) have clearly and ele-
gantly discussed the problem. Summarizing
their points, in discussing the evolution and
adaptive radiation of a group, one must estab-
lish that the group is monophyletic. To estab-
lish monophyly one must eliminate cases of
convergence. However, convergence 1$
surely the most underestimated problem in
systematic studies (Davis, 1979) and, in im-
perfectly known groups, one may be unable to
detect it. The problem of convergence be-
comes acute when one studies adaptive radi-
ation. As Cain (1964) pointed out, the pheno-
typic expressions we see are the result of
adaptations of an organism to its environ-
ment. Two snail species of different phylo-
genies may have similar looking shells be-
cause they live on rocks in rapidly flowing
water; they may, because of this environment,
have similar reproductive strategies and thus
the penis of both species may be similar,
gonadal morphology may be the same, and
other character states may be held in com-
mon as well.

If one can eliminate convergent taxa and
«establish monophyly for a group, the problem
of establishing clades arises. By clade, |
mean, the term as first used by Huxley (1959),
discussed in detail by Cain & Harrison (1960),
and demonstrated (with production of a
cladogram) using set theory analysis by
Wilson (1965). | do not refer to a neo-cladism
cherished with religious fervor by some prac-
ticing systematists, for whom a clade can
only be recognized by assessing relationships
among taxa on the basis of certain dogmatic
rules selecting primitive character states and
derived character states, grouping taxa on the
basis of shared derived character states, es-
tablishing sister groups, ignoring the fossil
record, and ignoring ecological factors as they
relate to adaptation.

The problem of recognizing and selecting
primitive character states has been thorough-
ly discussed (Cain, 1964; Cain and Harrison,
1960). | am distrustful of stating that a given

character state is primitive. If a character state
is widespread among species in a radiation,
some will call this character state primitive; |
think it unwise to do so for the following rea-
sons. A widespread character state may re-
flect the successful adaptation of organisms
to their environment because of that state.
The character state could have been derived
from a character state seen in only one spe-
cies where other species with the “primitive”
state are extinct because that character state
is now selected against in most microhabitats.
Some would consider the character state
seen in only one species to be unique and
thus derived. In essence, what is the direction
of evolution of certain character states in
question? The problem is compounded when
one realizes that in any systematic study
some of the useful characters are unordered
multistate characters. In the absence of a fos-
sil record, each choice for the primitive char-
acter state from among the unordered states
increases the probability of error. The sea-
soned neo-ciadist will respond that one
should do an outgroup comparison. If a char-
acter state is widespread in a group A and
also in outgroup B then surely this is the primi-
tive character state. However, if the first oper-
ation is to eliminate cases of convergence,
and if outgroup B converges on A and has
been eliminated from our assessment of the
course of evolution of A, then it would be
circular reasoning to state that a character
state widespread in A is primitive because it is
widespread in B. The distribution of this char-
acter state may simply result from the same
successful solution of adjusting to the same
environmental pressures in both groups
(Cain, 1964).

What can be done towards eliminating con-
vergence and establishing clades depends on
the data base available. If sufficient data are
available from the fossil record and/or from
geological events that give evidence for the
rates and direction of change, then one may
be able to say a great deal about clades and
phylogeny. On the other hand, if there are too
few data to allow for elimination of cases of
convergence and therefore for determining
cladistic affinities, all that may be possible is a
phenetic analysis (Cain & Harrison, 1960;
Hoagland & Davis, 1979). Unlike mammalo-
gists and ichthyologists, malacologists have
no fossil data for those suites of characters
that are essential for establishing the phylo-
geny of any group of mollusks. There are no
fossilized reproductive systems, digestive

INTRODUCTION ТО SYMPOSIUM 3

systems (exclusive of radulae), nervous sys-
tems, etc. As shell convergence is a major
problem in assessing cladistic relationships
among molluscan groups (Davis, 1979), itis a
most difficult task to discuss the phylogeny of
any group of mollusks objectively. The burden
of proof rests upon the data base.

In this symposium there are two papers
dealing with populations. One is on popula-
tions of the same species of lymnaeid gastro-
pod (Calow), the other on a population of a
single species of marine bivalve (Trueman).
These papers show ranges of adaptability of
populations to different types of environ-
mental pressure. Genetically controlled popu-
lation variability indicates adaptation under
varying conditions of environmental stress and
is essential for adaptive radiation. At the other
extreme, two papers involve evolutionary
trends in the phylum Mollusca, i.e. those of
Salvini-Plawen on the evolution of the mol-
luscan digestive system and of Haas on the
evolution of molluscan calcareous hard parts.

Of the 16 papers in this symposium, five
involve marine bivalve radiations with empha-
sis оп macroradiations. Four of these reflect
the comparative anatomical school of thought
established by C. M. Yonge while one (Hoag-
land & Turner) combines ecological and
molecular genetical data with morphometric
analyses to discern patterns of adaptive
radiation.

Seven papers involve gastropod radiations
and/or deployment; four are about marine
groups, two on land snails, and one on a
freshwater-amphibious group. Three of these
papers (McLean, Fretter et al., Houbrick)
present detailed anatomical data on a single
species. The species they describe are
enigmatic species, relicts important for under-
standing the possible relationships among
largely extinct marine radiations. These
papers and that given by Bouchet on the
Terebridae clearly show the relevance of
combining fossil data with neontological data
to assess modes and tempos of evolution and
adaptive radiation.

The land snail papers (Cain, Tillier) clearly
demonstrate the need for detailed ecological
studies in order to understand how pheno-
types reflect adaptations to different environ-
mental pressure. What have been described
as numerous species on the basis of the
usual standard systematic analysis often
reduce to one or a few species once one
discovers that subtle differences of rainfall,
altitude, and sympatry greatly affect shell

shape and size parameters within a single
species. Shell shape and size have been
widely used to describe species of land snails.

One paper (Davis) demonstrates that with
the ability to establish monophyly by eliminat-
ing convergent groups, and with paleonto-
logical and geological time markers, one may
indeed establish a phylogeny and assess the
direction, tempos, and modes of evolution
and adaptive radiation within a nearly world-
wide family. Two different modes and tempos
of evolution are discussed, one fitting a
punctuational model, the other a gradualistic
model.

In summary, in many of these papers the
reader will see the essential role of funda-
mental systematic studies for understanding
relationships among organisms. It is clear,
however, that an awareness and practice of
modern principles involved in ecology, evolu-
tion, macroevolution, and adaptive radiation
are essential if one aspires to understand the
origin, evolution, and adaptive radiation of any

group.
LITERATURE CITED

BRANCH, G. M., 1971, The ecology of Patella
Linnaeus from the Cape Peninsula, South Africa.
1. Zonation, movements and feeding. Zoologica
Africana, 6: 1-38, 5 pl.

BRANCH, G. M., 1974a, The ecology of Patella
Linnaeus from the Cape Peninsula, South Africa.
2. Reproductive cycles. Transactions of the
Royal Society of South Africa, 41: 111-160, 3 pl.

BRANCH, G. M., 1974b, The ecology of Patella
Linnaeus from the Cape Peninsula, South Africa.
3. Growth rates. Transactions of the Royal So-
ciety of South Africa, 41: 161-193.

BRANCH, G. M., 1975a, The ecology of Patella
species from the Cape Peninsula, South Africa.
4. Desiccation. Marine Biology, 32: 179-188.

BRANCH, G. M., 1975b, The ecology of Patella
species from the Cape Peninsula, South Africa.
Commensalism. Zoologica Africana, 10: 133-
162.

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4 DAVIS

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MALACOLOGIA, 1981, 21(1-2): 5-13

ADAPTATIONAL ASPECTS OF GROWTH AND REPRODUCTION IN
LYMNAEA PEREGRA (GASTROPODA: PULMONATA) FROM EXPOSED
AND SHELTERED AQUATIC HABITATS

P. Calow

Department of Zoology, University of Glasgow, Glasgow G12 8QQ, United Kingdom

ABSTRACT

Lymnaea peregra from wave-swept shores and fast-flowing streams were smaller than con-
temporaries from ponds and slow-flowing canals. Laboratory observations made on snails from
both types of habitat, under the same constant conditions, suggest that they did not differ
significantly in growth rate but that the snails from the sheltered habitats grew longer than the
others. This difference in growth pattern was associated with differences in reproductive pattern.
The snails from the exposed habitats, for example, initiated reproduction earlier and put more
effort into it than the snails from the sheltered habitats. These differences in growth and repro-
duction could be explained in terms of differences in selection pressure between habitats of
varying exposure. Conditions in exposed sites approximated to r-selection and conditions in

sheltered sites to K-selection.

INTRODUCTION

An adaptive radiation begins when popula-
tions become isolated in differing ecological
circumstances. Spatially limited bodies of
freshwater represent a uniquely available
series of natural experiments for investigating
this process. In these systems there are a few
species occupying a wide range of habitats
and showing a considerable degree of within-
species variation. It has been suggested that
such partial speciation, or radiation at the
species level, is due on the one hand to the
habitat isolation noted above and, on the
other, to the transitory (in terms of geological
time) nature of freshwater bodies which pre-
vents the process of radiation going far
enough to result in good species (Russell-
Hunter, 1970). In studying such within-
species variation, however, it is necessary
to distinguish genetically determined differ-
ences from those due to more immediate
environmental effects. It is also important to
distinguish between “random” variation and
that which can meaningfully be ascribed to
the process of adaptation.

Lymnaea peregra (Muller) is a widespread
freshwater animal which shows considerable
variation between populations, some of which
is correlated with the habitat type in which it is
found. Thus, individuals from exposed habi-
tats (shores of lakes and streams) are usually
smaller than individuals from sheltered habi-

(5)

tats (ponds, lakes and slow-flowing canals).
However, the extent to which these differ-
ences are genetically determined has been
the subject of some controversy. Bondesen
(1950), for example, refers to the small indi-
viduals from exposed sites as “hunger forms”
implying an environmental rather than genetic
cause whereas Boycott (1936) was convinced
that some of the differences in size could be
ascribed to genetic differences.

Using a technique in which snails from dif-
ferent populations were cultured under the
same, carefully controlled conditions | at-
tempt, in this paper, to distinguish between
these two hypotheses. | also attempt to ex-
plain the differences in growth pattern in
terms of the possible selection pressure ex-
perienced in each kind of habitat and to relate
the results to more general life-cycle theory.
In this way it may be possible to clarify the
general principles involved in radiation at the
species level as they influence life-cycle traits.

MATERIALS AND METHODS
a) Habitats and initial collection

Snails were collected, initially, from four
habitats: 1) an exposed shore on the banks of
Loch Lomond (Grid ref. NS 365965); 2) a
fast-flowing stream (flow > 50 cm зес-1)
entering Loch Lomond (Grid ref. NS 445905);

6 CALOW

3) a weedy portion of the Forth and Clyde
Canal (Grid ref. NS 635735); 4) the weeds of a
small, closed pond (Grid ref. NS 745605).
Sites 1 and 2 will be referred to as the “ех-
posed” habitats and sites 3 and 4 as the
“sheltered” habitats. Water movements in the
body of the canal were very slow
(< 5 ст зес-1) and were negligible in the
weed beds of this habitat.

All samples were taken in November. Large,
random collections (200-300 snails) were ob-
tained from each site. Since L. peregra is
semelparous all individuals were assumed to
be approximately the same age. Most snails
were killed on collection and stored in 4%
formalin and these were used for the analysis
of the initial size-frequency distribution. Here,
shell length (SL as defined in Russell-Hunter,
1961a & b) was taken as the index of snail size
and was determined to the nearest 0.1 mm
using vernier callipers.

b) Culture techniques

Observations in culture were restricted to
the stream and canal snails. Sixty (i.e. thirty
pairs) of the snails, from the initial sample
from each site, were kept alive and cultured in
pairs in perforated, perspex pots (150 ml) ina
water bath (total volume = 501) through
which water was recycled (100 ml per min.)
over activated charcoal and glasswool. The
water was prepared synthetically and was
equivalent to the “SSW medium” of Thomas
(1973). The pH of the medium stabilised at
around 8 and the conductivity was approxi-
mately 422 umhos ст-2. The medium from
the whole tank was replenished fortnightly.

Snails were fed weekly on cooked lettuce
(all prepared at the same time and stored
frozen until use) and at this time pots were
cleared of old food and faeces. Food was al-
ways in excess.

А constant temperature of 18(+2)°C
(measured in the perspex pots) was used
throughout. This is because preliminary ex-
periments on the growth and fecundity of
snails from the canal population had sug-
gested that the best performance would be
obtained at between 16 and 22°C. As temper-
ature increased and fell about this range,
growth rates and egg production rates re-
duced sharply. Similar results have been ob-
tained for other temperate lymnaeids (Van der
Schalie & Berry, 1972).

Using the above regime, the following pa-

rameters were measured: size of adults when
they began to spawn (they lay egg capsules
containing up to 100 eggs); capsule produc-
tion per adult per day; adult mortality. Fifty
capsules were collected in one week (approx-
imately one month after capsule production
had begun) from each group and were used
to determine the number of eggs per capsule,
hatching time and percentage hatchability.
Upon hatching a sub-sample of 100 hatch-
lings was used to determine initial size and a
further sub-sample of 50 snails (canal and
stream only) was set collectively in a 5001
tank with circulation and feeding regimes as
before. The large tank was divided into two
equal sections to accommodate sub-samples
from each of the populations. At first it was
also necessary to confine (using perforated
baffles) the small snails in a smaller portion of
the larger sections. As snails increased in size
the confinement was relaxed until at about
fifty percent of their full size, they were al-
lowed full access to the total volume of the
relevant section of the tank. Under these con-
ditions | measured SL, size when capsules
were first produced (SL), capsule produc-
tion per snail and adult mortality. Unlike the
first series of observations, snails could not be
identified individually, so size and fecundity
were measured as population averages.

At the end of the second laboratory genera-
tion, egg capsules were again collected from
each population and treated as before. A third
generation of hatchlings was cultured through
to adulthood, and measurements repeated as
above. Snails collected from the field were
referred to as generation 1, their progeny as
generation 2, and the progeny of these as
generation 3. In all generations, observations
on capsule production and adult mortality were
restricted to a five week period.

c) Energy budgets

Energy budgets were carried out on repro-
ductive adults in generation 2. Known weights
of lettuce were fed to ten individuals from
each habitat type and after a 24 hr period
snails were removed to clean water with no
food and the remaining lettuce was re-
weighed. Faecal pellets were collected from
the snails until no more “green” ones were
produced (usually 48 hr). Wet weight to dry
weight ratios of food and energy values of
food and faeces were estimated using stand-
ard techniques (Phillipson, 1964). Reproduc-
tive losses were determined from the energy

GROWTH AND REPRODUCTION IN LYMNAEA Z

values of hatchlings, again using bomb
calorimetry. All energy values were ex-
pressed in Joules (approx. 4.2 J/cal.).

RESULTS
a) Size of snails in field populations

The mean sizes of snails on collection were:
11.97 mm (SE = 1.94)—canal; 9.77 mm (SE
= 1.50)—pond; 6.37 тт (SE = 1.01)—
stream; 6.29 mm (SE = 1.08)—loch. Analysis
of variance, based on a completely random-
ised design, indicated that there were signifi-
cant differences in the data (F = 5.2,
Р < 0.01 for 3/167 df). Specific differences
between individual means were identified ap-
proximately using the “least significant range
test” of Sokal & Rohlf (1969) which defines
the least significant difference (LSR) allowed
at a given level of probability. LSR (P = 0.05)
for the data was approximately equal to 3.
Hence differences existed within but not be-
tween the “exposed” and “sheltered” habitat-
groups.

Because of differences in the physical form
of the four habitats it proved impossible to ob-
tain comparative density estimates for each of
the four snail populations. Subjectively,
though, it was clear that the density of the
pond and canal populations was much great-
er than the density of the stream and littoral
populations.

b) Growth

Typical of most freshwater snails, growth
under laboratory conditions was sigmoid
(Calow, 1973). Hence when the data were
plotted on semi-logarithmic co-ordinates (Fig.
1) there was an initial linear, exponential
phase after which size decelerated on to a
steady-state. The equations for the linear part
of the curve (first 10 weeks), based on all the
individual measurements, were:

Canal
Gen. 2: Log, SL = 0.169t - 0.151
Gen. 3: Log, SL = 0.174t — 0.181

Stream.
Gen. 2: Log, SL = 0.174t — 0.184
Gen. 3: Log, SL = 0.168t — 0.167

where: е = base of natural logarithms
(=2.718), SL = shell length (mm), t = time

(weeks). In these equations the regression
coefficients differed significantly from zero
(t > 10, P < 0.001) but not from each other
(t< 1, P > 0.05). Similarly the other con-
stants, representing SL at time zero, did not
differ significantly from each other (t< 1,
P > 0.005). Hence the snails from each popu-
lation had the same rates of growth over the
exponential phase (mean slope of regression
lines = coefficient of exponential growth =
0.171) and the same initial size.

However, mean steady-state SLs (SL.,) for
each group (estimated by eye and by extra-
polation) were approximately 14-18 mm for
the canal snails (all generations) and
9-12 mm for the stream snails (all genera-
tions). These differences are clearly seen in
Fig. 1 for generations 2 and 3. Snails from the
canal reached a larger final size than snails
from the stream.

c) Size at reproduction

Table 1 gives the mean sizes of snails in
the laboratory populations at the start of
capsule production for each of the three gen-
erations. Analysis of variance demonstrated
that significant differences occurred between
the mean sizes of snails from all four popula-
tions in generation 1. The LSR (P = 0.05) for
these data was 3.6 so that significant differ-
ences occurred between but not within the
“exposed” and ‘sheltered’ habitat groups.
Snails from the “exposed” habitats began to
produce egg capsules at a smaller, adult size
than snails from the “sheltered” habitats. This
difference was maintained between the canal
and stream populations over a further two
laboratory generations (Table 1).

The average size at maturity in the different
populations is marked in Fig. 1, and this
shows that reproduction began before growth
ceased in both groups.

d) Fecundity and viability of eggs

For the most part, information on fecundity
is restricted to the canal and stream popula-
tions.

Table 2 shows: (a) mean capsule produc-
tion per individual; (b) mean eggs per cap-
sule; (c) the average, total number of eggs
produced per individual per week (с = ах 5).
There was no significant difference between

8 CALOW

100
4 я
10 я О Q © о E
= Ô
> и
' a O
a à
Ф О
1 (0)
AS)
0-1
0 5 10 15 20 25
WEEKS

FIG. 1. Graph of log SL against time for canal snails (Gen. 2—A; Gen. 3—M) and stream snails (Gen. 2—0;
Gen. 3—A). Points are averages but the regression equations given in the text are based on individual
measurements. Arrows indicate times at which capsules were first discovered in the cultures.

the mean capsules produced per individual
between populations for any generation (t =
0.2 to 0.4, for > 9 df; P > 0.05) but the num-
ber of eggs per capsule was consistently
greater in the canal population (for gen. 1 and
2, >2:P"</0/05;for.gen:3,ti1.8P:<204).
Canal snails therefore produced the same
number of capsules over the experimental
period but a greater number of eggs than
stream snails. lt should be noted, however,
that capsule production and eggs per capsule
reduced with each successive generation in
both groups of snails; possibly a laboratory
effect. Correlated with the larger egg-load, the

capsules of the canal snails were significantly
longer (L) and wider (B) than the capsules of
the stream snails (а = 2 — 4; P < 0.05; grand
means: L = 15.98 (+1.08) mm for canal
snails and 10.35 (+ 1.4) mm for stream snails;
В = 3.41 (+0.4) mm for canal snails and 3.02
(+0.3) mm for stream snails).

| have no quantitative laboratory data on
capsule production from the littoral and pond
snails but a field survey over three years has
shown the mean eggs per capsule to be 17.1
(+4.3) and 29.8 (+2.1) in the littoral and pond
Snails respectively. These were significantly
different (4 = 4.1; Р < 0.001) as were the

GROWTH AND REPRODUCTION IN LYMNAEA 9
TABLE 1. Shell length (mm) at the onset of reproduction.
Gen. 1 Gen. 2 Gen. 3
Population Sic SE? N++ SL SE N SIL SE N
Canal 14.4 1.2 31 13.4 eat 32 12.9 1.3 31
Pond 12.8 1.0 30
Stream 8.1 lest 35 7.6 1.0 28 7.2 Vel 25
Littoral 8.4 1.0 37
F/d** 5.9 23 2.0
df 3/129
P 0.01 0.02 0.05
-—_—_—_—_—__—_ A _—_—__—_——______ —__—___—___ === ==>
+SL = shell length.
*SE = standard error.
++N = number of replicates.
**F for analysis of variance on four habitats; d for test of significance between two habitats.
TABLE 2. Reproductive output in snails from different habitats.
ЕЕ Е
(а) (5) (с)
Population Caps./ind./week Eggs/caps. Eggs/ind./week
AAA TAPA Е O ee
Canal
Gen. 1 1.67(+0.51) 32 (29) 52.10
Gen. 2 1.37(+0.43) 28.6(+3.3) 39.18
Gen. 3 1.09(+0.27) 23.3(+1.9) 25.39
average 38.89
Stream
Gen. 1 1.59(+0.33) 26.1(+2.2) 41.49
Gen. 2 1.29(+0.11) 22.3(+1.8) 28.76
Gen. 3 1.01(+0.10) 19.5(+2.3) 19.70
average 29.98

FOO

Confidence limits = 2 standard errors.

sizes of capsules from each habitat; L = 13.2
(+0.28) for pond snails and 5.8 (+0.48) for
the littoral snails (d = 19.5, P < 0.001), B =
3.55 (+0.32) for pond snails and 2.33 (+0.12)
for littoral snails (d = 2.8, P < 0.01). Clearly,
the capsules of the pond snails approximated
in egg content and physical dimensions to
those of the canal snails whereas the cap-
sules of the littoral snails were even smaller in
content and physical dimensions than the
stream snails.

Data on the hatchability and subsequent
size-at-hatching of snails from the stream and
canal populations are summarized in Table 3.
There was no significant difference in either
the time taken for eggs to hatch (ca. 12-13
days) or in the percentage hatchability of cap-
sules (са. 60-70%) or in the size of the snails
on hatching (ca. 0.86 mm SL; see also Fig. 1).

The percentage of adults surviving for the
five-week observational period in each con-
secutive year were са. 65, 56, 58 for the canal
population and 43, 50, 48 for the stream pop-
ulation. Hence, on average, adult survivorship
during the breeding period was greater for the
canal snails than for the stream snails. In both
groups, survivors continued to lay eggs for
some time after the five-week observational
period.

e) Energy budgets

The dry weight to wet weight ratio of lettuce
(from 30 determinations) was 0.17 (+0.03)
and the Joule equivalent was 15.3 (+2.8)
J mg”! dry weight. The mean amounts eaten
by the canal and stream snails were respec-
tively 54.83 (+6.43) and 35.69 (+4.98) J indi-

10 CALOW

TABLE 3. Hatchability, hatching time and size at hatching.

% Capsules hatching

Canal
Gen. 1 65.02
Gen. 2 73.31
Stream
Gen. 1 61.94
Gen. 2 71.44
F
df
Р

Time to hatch (days)

Size at hatching (mm)

13.92(+1.74) 0.84(+0.016)
12.11(+1.00) 0.85(+0.017)
13.09(+1.20) 0.84(+0.013)
11.67(+0.89) 0.89(+0.054)
1.91 0.0256
3/85 3/397
>0.05 >0.05

Confidence limits = 2 standard errors.

vidual-1 day-1 and these are significantly dif-
ferent (t = 5.22, Р < 0.001 for 19 df).

The partitioning of the input energy by the
snails is illustrated in Fig. 2. Absorption effici-
encies for both types of snail approximated to
60%. The respiratory losses were derived
from the equation of Berg & Ockelman (1959)
relating the fresh weight of L. peregra to oxy-
gen consumption at 18°C for snails taken from
the field in June. The mean fresh weights for
each experimental group of ten snails were
115.4 тд and 225.3 mg for the stream and
canal groups respectively. An oxy-joule equiv-
alent of 21 J/ml oxygen uptake was em-
ployed.

Reproductive losses were estimated from:

a (ash-free dry weight of hatchlings) joules mg” ! dry weight
B

where the mean ash-free dry weight for all
hatchlings was 0.0012 mg and the joule equiv-
alent was 23.1 Jmg-! ash free dry weight
(there being no differences between groups;
Р > 0.05). а was the mean number of eggs
produced per individual per day and was de-
rived from Table 2 and В was the efficiency of
conversion of freshly laid gametes to hatch-
lings and was taken to be 0.6 (Calow, 1979a).

That part of the budget unaccounted for
(= Rest) represents energy lost in egg cap-
sules, excreta and secreta (e.g. mucus;
Calow, 1977) and that available for somatic
growth. Of the absorbed energy most was
used in respiratory metabolism and of the
non-respired fraction of the absorbed energy
(N-RA) 30.73% was invested in reproduction
by the canal and 40.91% by the stream snails.
However, it is to be noted that these figures
will underestimate the investment in repro-

35-7)

EGESTA

RESP

54.8.
EGESTA
75

CANAL STREAM

FIG. 2. Percentage allocation of ingested energy
between egesta (faeces), respiration (Resp), re-
production (Rep) and other aspects of metabolism
(Rest—see text for further specification). Figures
over columns = energy ingested individual! day’.
Resp + Rest + Rep = absorbed energy. Rest +
Rep = non-respired fraction of absorbed energy
(N-RA).

duction since they do not include estimates
for the wall material of the capsule. Since
more of the latter is produced per egg of
stream than canal snails (see above) the dif-
ference between the proportionate invest-
ments in reproduction of these two groups is
likely to be more than suggested above.

GROWTH AND REPRODUCTION IN LYMNAEA ИЯ

DISCUSSION

Over the period of exponential growth, SL
doubled approximately once every four weeks
irrespective of whether the snails were derived
from the canal or stream populations. A similar
growth rate was recorded by Turner (1926)
who made observations in the laboratory
(under approximately the same temperature
conditions as those used here) on more than
30,000 snails (mainly of pond origin) over five
generations as part of the Boycott-Diver proj-
ect on the inheritance of sinistrality in L.
peregra (Boycott et al., 1930). The growth rate
of this species, when measured in the ex-
ponential phase and under constant condi-
tions, therefore seems to vary little from one
population to another.

Despite these similarities, between-popula-
tion differences did begin to occur in growth
after the inflexion of the growth curve. Stream
snails became reproductive at a smaller size
(SLrep) and hence earlier in time than the canal
snails and ultimately reached а smaller
steady-state size (SL..). The snails in the ex-
periments of Turner (1926) started producing
capsules at 10 mm SL but grew © а SL, of 15
to 19 mm and these results are similar to my
data on snails from the canal. SL,ep of the
Glasgow pond snails was also similar to the
results of Turner whereas the SL... of the lit-
toral snails conformed more closely to that of
the stream snails. It is possible, therefore, that
the growth strategies of the stream and canal
snails apply more generally to L.peregra in
“exposed” and ‘sheltered’ habitats respec-
tively. That is, in exposed conditions L.
peregra starts laying eggs earlier and reaches
a smaller final size than snails in sheltered
conditions.

As well as differences in the pattern of
growth and the timing of reproduction there
were differences between the stream and
сапа! snails in the amounts of eggs produced.
Canal snails had a higher fecundity (as meas-
ured by egg output per parent) than the stream
Snails and circumstantial evidence suggests
that similar differences occurred between the
pond andlittoral snails; the former correspond-
ing more closely to the canal snails and the
latter to the stream snails. However, since
there were differences in the sizes of the par-
ents at reproduction these apparent differ-
ences in absolute fecundity may not give a true
indication of the cost of reproduction to the
parents and energy budgets offer a better
measure (Hirshfield & Tinkle, 1975; Calow,

1978, 1979b). These, as summarised in Fig. 2,
suggest that stream snails invest more of their
N-RA in reproduction than the canal snails,
particularly if capsule walls are taken into ac-
count, and that in both groups there is little
residual energy for somatic growth once re-
production has been initiated. Hence the
stream snails trade-off growth for reproduction
more completely and at an earlier stage than
the canal snails. Furthermore they may also
trade-off adult survivorship for high reproduc-
tive effort (Calow, 1979b) since, in culture, the
stream snails are more mortality-prone than
the canal snails once reproduction has begun.

The major differences in phenological prop-
erties between the “exposed” and “sheltered”
populations, then, were size at reproduction
and probably reproductive effort. These differ-
ences were maintained under constant labora-
tory conditions over at least two generations
and so were likely to have been determined
genetically, not by proximate environmental
factors. Can they, therefore, be explained on
the basis of environmental variations that bring
about differences in selection pressure be-
tween the populations? Under “exposed”
conditions mortality is likely to be of an unpre-
dictable and age-independent kind due to
spates and wave action. Food supply may also
be unpredictable due to the scouring action of
water movement on encrusting algae (Calow,
1974), the major food of L. peregra (Calow,
1970). Hence it is likely that here selection will
have favoured early reproduction in terms of
both the size of snails and their age. This is
because restrictions in food supply might limit
the growth of the snails and necessitate repro-
duction at an earlier adult size and because
early reproduction is of clear advantage when
there is unpredictable, age-independent
mortality. For the same reasons, once begun,
as much effort as possible should be invested
in reproduction. Alternatively, under the more
predictable “sheltered” conditions it may be
advantageous to put breeding off in order to
“cash-in” on a larger absolute fecundity made
possible by a larger adult size. This is impor-
tant since selection operates on the basis of
eggs per parent not energy involvement in re-
production or any other index of reproductive
output.

Snails from “exposed” and “sheltered”
habitats also differed in the way they packaged
eggs into capsules in that the stream snails put
fewer eggs into smaller capsules than the
canal snails. The relative merits of these two
kinds of strategy are probably related to egg

12 CALOW

survivorship and the efficiency of using the
energy made available for reproduction.
Under “exposed” conditions, for example,
small capsules are probably less susceptible
to scouring and, since the loss of a capsule in
spate will be all-or-nothing the chances of the
loss of acomplete batch of all eggs produced
by an individual will be lessened by spreading
eggs between a larger number of capsules.
This trend, to produce physically small cap-
sules containing few eggs, was also observed
in the littoral snails. Alternatively the amount of
capsule membrane/egg will increase as cap-
sule size becomes reduced and since the
energy value of the membrane may not be
insignificant (Calow, unpublished) then the
number of eggs produced per unit energy
made available for reproduction will not be as
great for the small capsule-producers. For L.
peregra which occur in Loch Lomond, Russell-
Hunter (1961a & b) has suggested that there
may be polymorphism in capsule size (there
being large and small capsule morphs). Such
a genetic trait might reflect the occurrence of
semi-isolated populations living under differ-
ent conditions of exposure and wave action in
this large lake.

Finally, it is worth noting that the difference
in selection between “exposed” and “shel-
tered” conditions correspond approximately to
the differences envisaged in ‘r and ‘K’ selec-
tion (Pianka, 1970). The “exposed” conditions
approximate to ‘г’ conditions of selection in that
unpredictable mortality is likely to predominate
whereas “sheltered” conditions approximate
more closely to ‘K’ conditions of selection since
here density-dependent regulation is more
likely to dominate. Similar differences in the
nature and intensity of selection may also
occur within habitats where there is a cline in
exposure. For example, in the marine littoral
region, the upper shore is more exposed than
the lower and, interestingly, Spight & Emlen
(1976) have discovered exactly the same dif-
ferences in growth and reproduction in certain
marine gastropods occupying different parts of
the shore as those noted above for L. peregra
in different habitats. Thais lamellosa, a low
shore snail, grows for longer and produces a
larger clutch than Thais emarginata, an upper
shore snail. Of course, not all organisms in
exposed conditions will be subjected to the
same forces of selection. For example, some
species, like the freshwater river limpet
Ancylus fluviatilis, which lives in both fast-flow-
ing streams and on wave-swept shores, es-
capes the scouring action of water movements

by virtue of its streamlined shell and muscular
foot, and may be limited in population size
more by density-dependent constraints im-
posed by a poor food supply (Calow, 1974).
Similarly, littoral, freshwater triclads are limited
by density-dependent competition for a re-
stricted food supply (e.g. Reynoldson, 1966).
Hence, the sort of selection pressure experi-
enced by a population will depend not only on
the character of the environment but also on
the adaptive characters of the organisms
themselves (See also Calow & Woollhead,
1977).

REFERENCES CITED

BERG, K. & OCKELMAN, K. W., 1959, The respira-
tion of freshwater snails. Journal of Experimental
Biology, 36: 690-708.

BONDESEN, Р., 1950, A comparative morphologi-
cal-biological analysis of the egg capsules of
freshwater pulmonate gastropods. Natura
Jutlandica, 3: 1-208.

BOYCOTT, A. E., 1936, The habitats of freshwater
Mollusca in Britain. Journal of Animal Ecology, 5:
116-186.

BOYCOTT, А. E., 1938, Experiments on the artificial
breeding of Limnaea involuta, Limnaea burnetti
and other forms of Limnaea peregra. Proceed-
ings of the Malacological Society of London, 23,
101-108.

BOYCOTT, А. E., DIVER, С., GARSTANG, S. &
TURNER, Е. M., 1930, The inheritance of sinis-
trality in Limnaea peregra (Mollusca, Pulmonata).
Philosophical Transactions of the Royal Society
of London, Ser. B, 219: 51-131.

CALOW, P., 1970, Studies on the natural diet of
Lymnaea pereger obtusa (Kobelt) and its possi-
ble ecological implications. Proceedings of the
Malacological Society of London, 39: 203-215.

CALOW, P., 1973, On the regulatory nature of indi-
vidual growth: some observations from fresh-
water snails. Journal of Zoology, 170: 415428.

CALOW, P., 1974, Some observations on the dis-
persion patterns of two species-populations of
littoral, stone-dwelling gastropods (Pulmonata).
Freshwater Biology, 4: 557-576.

CALOW, P., 1977, Ecology, evolution and ener-
getics; a study in metabolic adaptation. Advances
in Ecological Research, 10: 1-62.

CALOW, P., 1978, The evolution of life-cycle strate-
gies in freshwater gastropods. Malacologia, 17:
351-364.

CALOW, P., 1979a, Conversion efficiencies in
heterotrophic organisms. Biological Reviews, 52:
385—409.

CALOW, Р., 19796, The cost of reproduction—a
physiological approach. Biological Reviews, 54:
2340.

CALOW, P. 8 WOOLLHEAD, A. S., 1977, The rela-
tionship between reproductive effort and evolu-

GROWTH AND REPRODUCTION IN LYMNAEA 13

tion of life-history strategies—some observations
on freshwater triclads. Journal of Animal Ecology,
46: 765-781.

HIRSHFIELD, M. F. & TINKLE, D. W., 1975, Natural
selection and the evolution of reproductive effort.
Proceedings of the National Academy of Sci-
ences, U.S.A., 72: 2227-2231.

PHILLIPSON, J., 1964, A miniature bomb calori-
meter for small biological samples. Oikos, 15:
130-139.

PIANKA, Е. R., 1970, on ‘г and ‘K’ selection. Атег-
ican Naturalist, 104: 592-597.

REYNOLDSON, T. B., 1966, The distribution and
abundance of lake-dwelling triclads—towards а
hypothesis. Advances in Ecological Research, 3:
1-71.

RUSSELL-HUNTER, W. D., 1961a, Annual уапа-
tions in growth and density in natural populations
of freshwater snails in the West of Scotland. Pro-
ceedings of the Zoological Society of London,
135: 219-253.

RUSSELL-HUNTER, W. D., 1961b, Life cycles of

four freshwater snails in limited populations in
Loch Lomond, with a discussion of intraspecific
variation. Proceedings of the Zoological Society
of London, 137: 135-171.

RUSSELL-HUNTER, W. D., 1970, Aquatic Produc-
tivity. Macmillan, London.

SCHALIE, VAN DER H. & BERRY, E. G., 1972, The
effects of temperature on growth and reproduc-
tion of aquatic snails. Sterkiana, 50: 1-92.

SOKAL, R. R. & ROHLF, F. J., 1969, Biometry.
Freeman, San Francisco.

SPIGHT, T. M. & EMLEN, J., 1976, Clutch sizes of
two marine snails with a changing food supply.
Ecology, 57: 1162-1178.

THOMAS, J. D., 1973, Schistosomiasis and the
control of molluscan hosts of human schisto-
somes with particular reference to self-regulatory
mechanisms. Advances in Parasitology, 11:
307-394.

TURNER, F. M., 1926, The rate of growth of
Limnaea peregra. Naturalist (Leeds) Aug. 1: 231-
235.

202

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MALACOLOGIA, 1981, 21(1-2): 15-21

RESPONSES OF AN ESTUARINE BIVALVE, SCROBICULARIA PLANA
(TELLINACEA) TO STRESS

E. R. Trueman and H. B. Akberali

Zoology Department, University of Manchester, Manchester, M13 9PL, England

ABSTRACT

The activity of Scrobicularia plana (da Costa)—an estuarine bivalve—has been monitored in
the laboratory, under simulated field conditions, by continuously recording valve movements,
heart rate and water flow. Rapid changes in environmental salinity (30-6°/) induce the re-
sponse of valve closure and inactivity which apparently effectively isolate the tissues from the
environment. Prolonged closure (<1 hr) results in anaerobiosis and an accumulation of acid
metabolites in the absence of ventilation of the mantle cavity. Whereas in low salinities the ionic
concentration of most ions in the body fluids decreases that of calcium ions increases. Experi-
ments with 45Ca using autoradiographic and counting techniques have demonstrated that the
calcium ions are derived from the interior of the valves. Similar behaviour has been observed in
respect to copper pollution. The ability to close the valves and to remain isolated from the
environment for up to 7 days suggests that Scrobicularia is particularly well adapted to withstand
the stresses of estuarine life whether these are changing salinity or pollutants.

INTRODUCTION ©

Scrobicularia plana (da Costa) is an estu-
arine bivalve found abundantly in intertidal
muds. Its behaviour in respect of heart rate,
pumping, valve movements and oxygen con-
sumption have been monitored in the labora-
tory under conditions simulating the natural
habitat and in the field in respect to heart rate
(Earll, 1975; Akberali, 1978; Akberali &
Trueman, 1979). In many bivalves studied,
e.g. Mya, Mytilus, Ostrea (Thompson &
Bayne, 1972; Walne, 1972), changes in
pumping activity elicit little variation in the
heart rate, but in Scrobicularia the heart rate
and amplitude fall markedly with reduction of
pumping. During activity, periods of pumping
(30—60 min.) alternate with ventilatory pauses
and the reduction of heart rate, e.g. 20-5
beats min-1, is observed to correspond with
the cessation of pumping (Fig. 1). During
longer periods of apparently spontaneous
quiescence (2=4-12 hr duration) pumping
ceases, the valves close, bradycardia occurs
and in some instances the heart beat com-
pletely ceases (Fig. 1C).

The purpose of this article is to consider
recent work on the behaviour and physiology
of Scrobicularia as they are affected by the
stress of changing salinity or by the presence

of pollutants. The ability of this species to de-
tect and to respond to adverse environmental
changes, such as may be found in estuaries,
will be reviewed. The response to stress con-
ditions is commonly valve closure and isola-
tion of the tissues from the external habitat.
This may, in Scrobicularia, be sustained for at
least seven days and the effectiveness of this
mechanism, as an adaptation to estuarine life,
is assessed.

home nas

et sport ph amet AYR tee nan ON

Minutes

FIG. 1. Examples of recordings of the heart beat of
Scrobicularia plana during А, activity; В, ventilatory
pause; and C, quiescence.

(15)

16 TRUEMAN AND AKBERALI

METHODS

The details of the methods used in these
investigations have been presented fully in
previous articles and it is only intended to
refer briefly to these. Activity of the clam was
recorded on a pen recorder in respect of valve
movements and heart rate by use of the im-
pedance technique (Trueman et al., 1973)
and gill pumping by a thermistor flow meter in
the exhalant water current (Foster-Smith,
1976). The flow meter was used simply as an
‘on/off’ detector, no attempt being made to
calibrate the instrument for the amount of
flow. Estimation of oxygen and carbon dioxide
in mantle cavity water was carried out on
samples withdrawn by hypodermic needle
from between the valve margins by use of a
Radiometer PHM 73 Blood gas analyser.
Each animal was discarded after the sample
was withdrawn (Akberali & Trueman, 1979).
The pH of the mantle cavity water was moni-
tored on a pen recorder using a microelec-
trode (Pye, Ingold) inserted in the mantle cav-
ity through a fine hole drilled in the shell. Cal-
cium ions present in the various body fluids
were measured using an Atomic Absorption
Spectrophotometer with EDTA added to the
extracts to a final concentration of 0.78% to
prevent phosphate interferences. The fate of
calcium previously incorporated into the shell
during stress situations was investigated by
placing Scrobicularia, with the outer surface
of the valves protected by varnish, in sea
water to which “°Са had been added. After 48
hours in unlabelled sea water to flush out “Ca
from the mantle cavity and extrapallial fluids
the clams were subjected to a standard salini-
ty stress by immersion in 20% sea water (S =
6°/..) whilst controls were left in normal sea
water. Valves from animals of both groups
were thoroughly scrubbed, dissolved in dilute
hydrochloric acid, prior to the 45Ca content be-
ing measured (Akberali, 1980).

Animals were collected fortnightly from
Morecambe Bay, transported to Manchester
University and kept in an aquarium at 10°C
during all experiments. A standard salinity
stress was applied by a sudden reduction of
salinity from normal to 20% sea water (30°/..-
67/00). Studies on the effect of copper pollution
were carried out in normal sea water to which
copper was added from a stock Cu (NO:)
solution to give predetermined final concen-
trations (Akberali & Black, 1980).

EXPERIMENTAL OBSERVATIONS

Application of rapid changes of salinity of
the medium in the form of a standard salinity
stress to Scrobicularia results in valve closure
and inactivity whilst the tissues are effectively
isolated from the surrounding water (Fig. 2).
During this stress, Scrobicularia, in common
with other bivalves, respires anaerobically
and produces succinic acid, alanine and other
volatile fatty acids (De Zwaan & Wijsman,
1976). Adverse environmental conditions,
such as aerial exposure, salinity or pollutant
stress, can cause Scrobicularia to close its
valves for periods up to 7 days with only short
and occasional pumping activity (Fig. 2). After
this period of salinity stress, pumping activity

HOURS

FIG. 2. Recordings of the valve movements of
Scrobicularia plana immediately following transfer
directly from 100% sea water at 0 hr to 20% sea
water: records A to D are 4 hr sections of a continu-
ous 168 hr recording which have been selected to
show events described in the text; traces are of two
individual Scrobicularia recorded simultaneously.

RESPONSES OF SCROBICULARIA TO STRESS 17

gradually increases in duration to more than
50% of the time as the clams come into equi-
librium with the external medium (Akberali,
1978).

It should not, however, Бе assumed that
during periods of stress the valves are always
tightly closed, completely sealing the animal
off from the habitat. The pO, in the mantle
cavity of Scrobicularia falls from 140 to about
50 mm Hg in 2 hr after valve closure but at
about 3 hr a temporary increase of 20 mm Hg
occurs (Fig. 3). This is probably due to a slight
opening of valve and mantle margins allowing
diffusion, for it does not occur when the valves
are forcibly sealed. Over the same period the
pCO, increases from 2 to 10 mm Hg, when
the valves are forcibly sealed, but only to
about 5mm Hg when the clam is being af-
fected by salinity stress alone. This suggests
that lower levels may be stabilised by outward
diffusion. During aerial exposure Scrobicu-

de м aca Nude, |

D
ae
Е
Е
a
O
a

fo, mm Hg

Hours

FIG. 3. PO2 and PCO levels in the mantle cavity of
normal (@—@) and forcibly closed (О---О)
Scrobicularia when transferred directly trom sea
water to 20% sea water at 0 hr. Each point is a
mean for 6 animals, which were then discarded.
Bars represent S.E.

laria shows a comparable increase in the
oxygen content after 3 hr except when the
valves are forcibly closed (Fig. 4).

To effect these changes in oxygen tension
when the valves are apparently closed the
mantle must be in contact with the media
along a narrow margin between the valves.
When the valves are closed, Scrobicularia
gives a rapid response to the change of salin-
ity or pollutants of the surrounding water
(Akberali & Black, 1980). This is presumably
because of the mantle being in contact with
the medium, so allowing the clam to exploit
conditions of minimum stress fully as they oc-
cur. This is advantageous in an estuarine en-
vironment where conditions are continuously
changing.

When Scrobicularia is transferred from
30°/ to 6°/..' aerated seawater the concen-
tration of ions, except Ca++, in the mantle
cavity fluid and blood falls to the level of the

ие
25
ЕС
N
о
ad 4
0
140
120
o 100
ЗЕ
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N
©

Hours

FIG. 4. PO ¿and PCO: levels of mantle cavity water
of Scrobicularia when placed at 0 hr in air (@ —@),
in atmosphere of nitrogen (№ — №) or in air with
valves forcibly closed (О---О). Each point a mean
of 7 animals, which were then discarded. Bars rep-
resent S.E.

18 TRUEMAN AND AKBERALI

external medium within 14 days (Akberali et
al., 1977). The blood calcium rises (Fig. 5) in
concentration to a maximum of 30 mM (about
х 3 that in normal sea water) within 5-7 days
when it drops towards that of the external
medium, stabilising at a new low level at
about 18 days (Akberali et al., 1977). Similar
changes are observed in extra-pallial and
mantle cavity fluid. To determine whether the
increase of calcium over the first 7 days is
related to anaerobic metabolism, clams were
placed in oxygen-free sea water where they
exhibit only a slight rise in calcium levels (Fig.

28
days

FIG. 5. Calcium concentrations of Scrobicularia
transferred directly from 100% sea water at day 0 to
20% sea water, mantle cavity water, (№ — №);
blood from the ventricle, (@—@); medium
(A — А). Each point is the mean of four determina-
tions made on samples pooled from 12-14 individ-
ual Scrobicularia selected randomly.

Sealed
lo

100/-N,
ha

20/-N,
1B

>
o

Са’ mM/I

24
days

FIG. 6. Calcium concentrations of Scrobicularia
placed in oxygen-free 100% sea water (A). After 6
days, the clams were additionally subjected to
salinity stress, by immersion in oxygen-free 20%
sea water (B and C). After 7 days the valves of
20 animals were forcibly closed (D). Mantle
cavity water, (№ — №); blood from the ventricle,
(0 — @); medium, (A— A).

6). Only when the valves are closed by im-
mersion in 20% sea water and the mantle
cavity not ventilated do calcium levels in-
crease markedly. Forcible closure of the
valves results in a rapid increase of calcium
over 2 days to about the same level as that
reached by animals in 20% aerated sea water
in 7 days. Continuous flow of oxygen-free
100% sea water through the mantle cavity,
may explain the absence of a significant rise in
calcium ions (Fig. 6, A-B) for in this condition
no anaerobic metabolites would accumulate
and no buffering would be required. The calci-
um ions have been shown to be derived from
the interior of the valves of the shell by disso-
lution during stress using 45Са and autoradi-
ographic and counting techniques (Akberali,
1980). The deposition of 4Ca by unfed
Scrobicularia, in which the outer surfaces of
the valves are painted with varnish to reduce
absorption of calcium, was estimated to be
0.228 ng 45Са per valve for a 72 hr experi-
mental period. When these clams are sub-
jected to the standard salinity stress about
50% of the incorporated 45Ca is lost within the
first 24 hours (Fig. 7). This suggests that the
freshly deposited calcium is more labile than
the remainder of the valve and is lost initially
in stress conditions. With longer term stress
(21 days) a greater demand for calcium may

12 + VE. + + 2
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1 2 3 4 5 6 7 14

DAYS

FIG. 7. Scrobicularia with their valves covered with
amyl acetate varnish left for 72 hours in 45Ca-
labelled sea water (5 wCi/L) for incorporation of
labelled calcium in the valves, followed by placing
those clams in unlabelled sea water for 48 hours,
the clams were then either subjected to a salinity
stress at day O for 14 days (@ — ®) or placed т
normal sea water as a control (@--@); values are
presented as means of total 45Ca counts per min-
ute (cpm) per valve (n = 8); bars represent S.E.

RESPONSES OF SCROBICULARIA ТО STRESS 19

TABLE 1. Animals were transferred directly from 100% to 20% sea water at 0 hr. At various intervals the
animals were removed and the calcium content of the mantle cavity fluid measured. The shell valves were
weighed and the area recorded. The shell valve was broken (shell crushing force) in compression between
the plates of an Instron 1122 standard mechanical testing machine with the kind cooperation of Prof. Currey,

University of York. Standard deviation in brackets. N.S. not significant.

Mantle cavity fluid Shell weight Shell crushing force
Са++ Con. mM/L gms/sq cm. Newtons/sq cm.
Period n=7 n = 14 n = 14
O hr. 10.32 (0.31) 0.1791 (0.015) 3.4641 (0.92)
24 hr. 11.64 (1.26) 0.1764 (0.028) 3.8284 (1.02)
Р < 0.02 N.S. N.S.
72 hr. 18.44 (4.40) 0.1671 (0.013) 2.7753 (0.97)
Р < 0.001 P= 0102 N.S.
7th day 23.79 (6.57) 0.1627 (0.011) 3.0256 (0.80)
Р < 0.001 Р < 0.002 М.5.
14th day 9.20 (10.13) 0.1563 (0.028) 3.0290 (0.84)
N.S. Р < 0.01 N.S.
21st day 5.45 (2.16) 0.1535 (0.013) 3.0148 (0.82)
Р < 0.002 Р < 0.001 М.5.

lead to the mobilisation of more tightly bound
calcium and gives rise to a significant de-
crease in shell weight but no apparent reduc-
tion in strength (Table 1).

Other behavioural features may be related
to the removal of metabolites derived from
periods of valve closure. During short term
stress periods (4-7 hr) and natural periods of
quiescence the pH of the mantle cavity water
falls from 7.8 to 7. This is probably due to the
accumulation of acid metabolites. A common
feature of recovery in Scrobicularia and other
species is the repeated sharp adduction of the
valves and overshoot of the heart rate. A brief
interval (ca 30 s) after each adduction the pH
of the mantle cavity of Scrobicularia falls
markedly to be followed by a slow rise as cili-
ary ventilation continues (Fig. 8). Similar step-
wise changes of pCO, and pO, occur during
recovery from longer periods of anaerobiosis
(circa 7 days) and imply intermittent recovery
compatible with hyperventilation caused by
valve adduction (Akberali & Trueman, 1979).
Simultaneous pressure pulses are generated

in both mantle cavity and tissues at adduction
resulting in outflow of water from the mantle
cavity (Trueman, 1966). However, the pres-
sure lasts longer in the tissues (1-2 $) than in
the mantle and could well bring about rapid
flushing out of metabolites from the tissues
whilst between adductions normal ciliary
pumping would remove these from the mantle
Cavity.

Scrobicularia responds to copper in solu-
tion in sea water at concentrations of
0.01 ppm in a manner similar to Mytilus
(Davenport, 1977) and other bivalve molluscs
(Manley & Davenport, 1979). Siphonal retrac-
tion and valve closure are the initial response
followed by a rapid drop in heart rate (Akberali
& Black, 1980). In concentrations in sea water
of 0.05—0.01 ppm copper in sea water the
clams begin to interact with the medium after
two to three hours. In 0.5 ppm the valves re-
main closed and the heart rate is maintained
at a low level over a 6 hr exposure period (Fig.
9). Replacement of the polluted water by
normal sea water even with the highest con-

> 5 Min

FIG. 8. Rapid valve movements (sharp rise representing adductions) observed shortly after transference to
sea water after exposure to a salinity stress for 24 hours. These valve movements correspond to a stepwise
increase in the pH of the mantle cavity water. With commencement and continuation of activity, pH returns to
normal.

20 TRUEMAN AND AKBERALI

A B

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RCE +h я 4 .
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Hours Hours

FIG. 9. Heart rate (H.R.) of Scrobicularia subjected
to various copper concentrations over the 6 hr ex-
posure period. A, 0.5 ppm; B, 0.1 ppm; C, 0.05 ppm
and D, 0.01 ppm copper concentrations in sea
water (S, 31°/.). Addition of copper solution indi-
cated by arrow (4), replacement with normal sea
water. Horizontal bars (am) refer to increased ac-
tivity in heart-rate and valve movements during the
6 hour exposure period. Vertical bars represent the
range of individual variation ( | ).

centration of copper used (0.5 ppm), leads to
recovery within 10-15 min, the valves open-
ing with an overshoot in the heart rate.

DISCUSSION

Mobilisation of calcium from the shell in
order to buffer the end products of anaerobic
respiration is a relevant physiological adapta-
tion to salinity stress or pollution since the
animals can protect the tissues by valve
closure for short periods, while sustaining
basal metabolism by anaerobiosis (Akberali,
et al., 1977; Akberali, 1980). However, with
longer exposure to copper (8 days), the clams
apparently have to interact with the medium to
flush out excretory and respiratory end-
products and when they open in 0.5 ppm
copper, poisoning takes place and as a result
mortality occurs (Akberali 4 Black, 1980).
Scrobicularia, when subjected to low salinity
stress, begins to interact more freely with the
medium after 5-7 days (Akberali, 1978). It is
possible that this is a critical period since de-
pletion of energy resources or accumulation

of metabolites may then necessitate valve
opening and interaction with the medium.

The ability of Scrobicularia to close the
valves and to remain effectively isolated from
the environment and yet to continue to re-
spond to external changes suggests that this
clam 15 particularly well adapted to withstand
the stresses of estuarine life whether these
are of changing salinity or pollutants. Such
adaptations in behaviour and their physiologi-
cal consequences are necessary for success
in an estuarine environment and the adapta-
tions required to avoid salinity stress appear
to be equally effective against pollutants pro-
vided the application is of similar relatively
short duration.

Rapid detection of pollutants in solution is
clearly of prime importance to the species.
The siphon of Scrobicularia reacts to copper
ions in the same manner whether isolated or
in preparations of the whole clam and it ap-
pears that this may be due to copper affecting
the neuromuscular junctions (Akberali &
Trueman, unpublished). In contrast to the di-
rect action of copper on the tissues, the sense
organ in the cruciform muscle complex, rec-
ognised by Odiete (1978) to respond to pol-
luted water, has recently been shown in our
laboratory to be the site of detection of zinc
ions in solution (Akberali, Wong & Trueman, in
prep.). The cruciform muscle complex is lo-
cated at the base of the siphons near the
mantle margins, where it may readily function
as a chemoreceptor organ in respect of water
drawn into the mantle cavity.

ACKNOWLEDGEMENTS

We are grateful to Drs. lles and Jones of
the Department of Zoology, Manchester Uni-
versity, for critically reading the manuscript.
These investigations have been supported by
N.E.R.C. Research Grant GR3/3436.

REFERENCES CITED

AKBERALI, Н. B., 1978, Behaviour of Scrobicularia
plana (da Costa) in water of various salinities.
Journal of Experimental Marine Biology and
Ecology, 33: 237-249.

AKBERALI, H. B., 1980, 4°Calcium uptake and dis-
solution in the shell of Scrobicularia plana (da
Costa). Journal of Experimental Marine Biology
and Ecology, 43: 1-9.

AKBERALI, Н. В. 8 BLACK, J. E., 1980, Behavioural
responses of the bivalve Scrobicularia plana (da

RESPONSES OF SCROBICULARIA TO STRESS 21

Costa) subjected to short term copper (Cu Il) con-
centrations. Marine Environmental Research, 4:
97-107.

AKBERALI, H. B., MARRIOTT, K. R. M. & TRUE-
MAN, E. R., 1977, Calcium utilization during
anaerobiosis induced by osmotic shock in a bi-
valve mollusc. Nature, 256: 852-853.

AKBERALI, Н. В. & TRUEMAN, Е. R., 1979, PO,
and PCO, changes in the mantle cavity of
Scrobicularia (Bivalvia) under normal and stress
conditions. Estuarine, Coastal and Marine Sci-
ence, 9: 499-507.

DAVENPORT, J., 1977, A study of the effects of
copper applied continuously and discontinuously
to specimens of Mytilus edulis (L.) exposed to
steady and fluctuating salinity levels. Journal of
the Marine Biological Association of the United
Kingdom, 57: 63-74.

EARLL, R., 1975, Temporal variation in the heart
activity of Scrobicularia plana (da Costa) in con-
stant and tidal conditions. Journal of Experiment-
al Marine Biology and Ecology, 19: 257-274.

FOSTER-SMITH, R. L., 1976, Some mechanisms
for the control of pumping activity in bivalves.
Marine Behaviour and Physiology, 4: 41-60.

MANLEY, A. R. & DAVENPORT, J., 1979, Behav-
ioural responses of some marine bivalves to
heightened sea water copper concentrations.

Bulletin of Environmental Contamination and
Toxicology, 22: 739-744.

ODIETE, W. O., 1978, The cruciform muscle and its
associated sense organ in Scrobicularia plana
(da Costa). Journal of Molluscan Studies, 44:
180-189.

THOMPSON, R. J. & BAYNE, B. L., 1972, Active
metabolism associated with feeding in the mussel
Mytilus edulis L. Journal of Experimental Marine
Biology and Ecology, 9: 111-124.

ТАЧЕМАМ, Е. В., 1966, Fluid dynamics of the bi-
valve molluscs Mya and Margaritifera. Journal of
Experimental Biology, 45: 369-382.

TRUEMAN, Е. В., BLATCHFORD, J. G., JONES, Н.
D. & LOWE, G., 1973, Recordings of heart rate
and activity of molluscs in their natural habitat.
Malacologia, 14: 377-383.

WALNE, P. R., 1972, The influence of current
speed, body size, and water temperature on the
filtration rate of five species of bivalves. Journal of
the Marine Biological Association of the United
Kingdom, 52: 345-374.

ZWAAN, A. DE & WIJSMAN, T. C. M., 1976, Review.
Anaerobic metabolism in Bivalvia (Mollusca).
Characteristics of Anaerobic metabolism. Com-
parative Biochemistry and Physiology, ser. B,
54: 313-324.

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MALACOLOGIA, 1981, 21(1-2): 23-34

ON ADAPTIVE RADIATION IN THE PECTINACEA WITH А
DESCRIPTION OF HEMIPECTEN FORBESIANUS

C. M. Yonge

Department of Zoology, University of Edinburgh,
West Mains Road, Edinburgh EH9 3JT, United Kingdom

ABSTRACT

Evolution of the highly efficient monomyarian condition in the Pectinacea is followed through
stages represented now by the heteromyarian (and so byssally attached) Mytilacea and the
similarly attached but less specialized monomyarian Pteriacea (e.g. Pinctada).

The Pectinacea are pleurothetic, posture being controlled by the left (upper) statocyst. The
inner ligament layer forms a spherical elastic pad responsible for the very wide gape; the inner
mantle margin (“velum”) is correspondingly enlarged. Increase in the ratio of striated ("quick") to
smooth (“catch”) muscle in the adductor is considered to be initially connected with expulsion of
pseudofaeces. Pallial eyes are possessed regardless of habit and are regarded as initially
associated with the wide gape and so danger from predators. Anterior as well as posterior
expulsion of pseudofaeces accounts for the complex lip apparatus and provides the means of jet
propulsion.

In habits the early separated Propeamussiidae, attached or free, without eyes or lip apparatus,
and some carnivorous, exploit abyssal depths. The Pectinidae are initially attached by byssus,
this further developed in Pedum and in Hemipecten (here first fully described and compared with
the Anomiacea), each associated with scleractinian corals; this habit replaced by freedom as in
Pecten and Amusium and by cementation in Hinnites. The same habit is attained earlier in life in
the Spondylidae, this family differing in hinge and ligament, the outer ligament layers moved
inward and replaced by fused periostracum with accompanying acquisition of ball-and-socket

hinge teeth.
INTRODUCTION KEY FOR ABBREVIATIONS ON FIGURES

This paper represents the association of in- a anus
formation and deductions on the Pectinacea adc adductor, smooth muscle
contained in a series of papers extending over adq adductor, striated muscle
many years (Yonge, 1936, 1951, 1953, 1967, aol anterior outer ligament layer
1973, 1975). More recent work, primarily on aur auricle (of right side)
the ligament, has shown that the Plicatulidae, by byssal strands
despite superficial resemblance by way of byn byssal notch
secondary ball-and-socket teeth to the ct ctenidium
Spondylidae, should be removed from the dd digestive diverticula
Pectinacea and associated with the Dimyidae e eyes (on middle marginal fold)
(Yonge, 1978a) in a new superfamily Plica- f foot
tulacea! (Yonge, 1975, 1977a). But the ex- Ш | fused inner marginal folds
tent of radiation with the family Pectinidae has fl fused lips
been increased by new observations herein if inner marginal fold
recorded, on structure and mode of life in il inner ligament layer
Hemipecten forbesianus Adams & Reeve, Ip labial palp
1850. pc pericardium

TWaller (1978) does not accept this separation of Plicatula from the Pectinacea nor the differences between ligamental
structure in the Pectinidae and in the Spondylidae. But criteria differ profoundly, those of palaeontology rest on the nature of
the secreted shell while those of comparative anatomy must be based on the nature of the secreting epithelia.

24 YONGE

pol posterior outer ligament layer
pr pedal retractor (of left side)

r rectum
so sense organ
V ventricle

ут visceral mass

EVOLUTION OF THE PECTINACEA

The Bivalvia, it is postulated, are primarily
infaunal molluscs with anterior and posterior
adductors formed by cross fusion of pallial
muscles at each end of a laterally com-
pressed body (Yonge, 1953, 1978b). Attach-
ment of the mantle lobes near the margin of
the shell (found in no other Mollusca) results
from muscular development in the innermost
of the three marginal folds which is concerned
with control of the increased water flow pro-
duced by the hypertrophied bivalve ctenidia.
Calcification, it is further maintained, followed
compression with an uncalcified mid-dorsal
region forming the ligament—thus the means
of opening the valves appeared pari passu
with the means of closing them.

Subsequent evolution in a diversity of bi-
valves and by a variety of routes led to loss of
the anterior adductor, and reorganization of
the organs around the remaining enlarged
and centrally placed muscle. This change to a
monomyarian condition has been achieved
with outstanding success in the order
Pterioida of the subclass Pteriomorpha (clas-
sification of Newell, 1965). Evolved in the
Ordovician this process culminated in the ap-
pearance of the Pectinacea which, including
the ubiquitous and outstandingly successful
scallops, represent one of the peaks of suc-
cess within the Bivalvia. The course of evolu-
tion must have proceeded by way of a hetero-
myarian condition which, wherever it appears,
involves byssal attachment and change from
infaunal to epifaunal life (Yonge & Campbell,
1968). At this stage the evolving mono-
myarian could have resembled the modern
Mytilacea. This is presumed to have been fol-
lowed by a preliminary, also byssally at-
tached, monomyarian condition, the organs
now reorganized around the central adductor
and with limited bilateral asymmetry. This
condition may have resembled that now pres-
ent in the least modified of the modern
Pteriacea, genera of the family Pteriidae such
as Pinctada.

The ultimate monomyarian condition involv-
ing greater reorganization around the central

adductor with assumption of a pleurothetic
habit—the sagittal plane now horizontal—and
with great modification of hinge and ligament
appears in the Pectinacea, also byssally at-
tached initially. Far from representing finality,
this highly specialized body form and habit was
the starting point for a striking range of diverg-
ing adaptations which it is the purpose of this
paper to describe. Later, at the end of the
Palaeozoic, the similarly monomyarian, but
byssally cemented Anomiacea were to dis-
play equally impressive adaptive radiation in-
volving the appearance of the limpet-like
Enigmonia and the completely free although
immobile Placuna (Yonge, 1977b).

The major alterations involved in change
from the heteromyarian to the initial mono-
myarian (pteriacean) condition are shown in
Fig. 1. The heteromyarian is equivalve but
inequilateral, the anterior pedal retractors
reduced. In the monomyarian, apart from loss
of the reduced anterior adductor, there is
change in shell shape from the inevitable tri-
angular form of the heteromyarian to the
laterally flattened and circular form of the
monomyarian. The reduced foot being
morphologically mid-ventral, almost the entire
widely open mantle cavity is posterior. In the
adductor the striated muscle component is
much the larger due to need for frequent ex-
pulsion of pseudofaeces which collect oppo-
site the posterior end of the ctenidia (Herd-
man & Hornell, 1904). The foot retains its
locomotory function in young stages but in the
adult is exclusively concerned with secreting
and planting the byssal threads that emerge
through a notch in the right valve, the animal
inclining towards that side. Both right pedal
retractors are reduced. Immobilized by the
presence of the large byssus, the foot can
have no cleansing function, only in the elongat-
ed Malleus is along, very active accessory foot
available for this purpose (Yonge, 1968). The
nervous system is that of a typical bivalve
(Herdman & Hornell, 1904).

It is easy to see how modification of shell
form with a central adductor influences the
disposition of both pallial and visceral organs
but not how the ligament could alter. That of
the heteromyarian is extremely opisthodetic
with a greatly enlarged posterior outer layer
extending over the full length of the inner
layer, the anterior outer layer reduced to
a vestige (Yonge & Campbell, 1968). The
Pteriacea have a long hinge line but it is
secondarily amphidetic with anterior outer,
middle and posterior outer layers all about the

PECTINACEA AND HEMIPECTEN FORBESIANUS 25

ssh

FIG. 1. Comparison between inequilateral heteromyarian (mytilacean) condition and the inequivalve
monomyarian (pteriacean) condition, viewed from left side (A, C) and in transverse section from posterior end
(В, 0), showing adductors, foot with retractors and byssus, ligament layers and ctenidium. Striated and
smooth muscle in adductor (C) denoted respectively by fine and coarse stipple. Solid arrows indicate sites of
inhalant and exhalant currents, broken arrows those of pseudofaecal extrusion. For key to abbreviations see

p. 23-24.

same length (Fig. 1C). This could not have
evolved from the extreme opisthodetic condi-
tion of the Mytilacea but, of course, within that
superfamily the heteromyarian condition
represents the end point of an evolutionary
trend. The necessarily heteromyarian ances-
tors of monomyarians must be envisaged as
less committed and the original, largely
amphidetic condition as being more easily
regained.

STRUCTURE IN THE PECTINACEA

In this highly modified monomyarian super-
family the animal becomes bilaterally asym-
metrical, always resting on the right side.
Even although the valves may be very similar,
the pleurothetic habit involves a functional
asymmetry. This was originally demonstrated

by Buddenbrock (1911, 1915) who showed
that in “Pecten” (actually largely species of
Chlamys) although both statocysts persist the
nerves from both mantle lobes are associated
exclusively with the better developed left
statocyst. Attached individuals always settle
on the right side, unattached ones turn over
on to that side if displaced. The highly special-
ized ligament is another basic feature. The
inner ligament layer is condensed into a char-
acteristic spherical rubber-like pad. This, as
pointed out by Trueman (1953a,b) is less
calcified than in the majority of bivalves which
accounts for its high modulus of elasticity.
Alexander (1966) further described it as an
“elastic block of amorphous cross-linked
protein, plasticized with water” and acting as
“a very efficient compression spring working
in antagonism to the adductor.” These and
other observations on this structure have

26 УОМСЕ

been made on species of Chlamys and
Pecten particularly in relation to their swim-
ming habits. Certainly it is one of the struc-
tures that have made swimming possible but
this ligament is no less developed in species
that are byssally attached or cemented. It
permits an unusually wide gaping of the
valves. The remainder of the straight edentu-
lous hinge line is occupied by long stretches
of anterior and posterior outer ligament layer
(this with the exception of the Spondylidae as
noted later).

Wide separation of the valves involves
changes in the mantle margins. The inner
muscular mantle fold with fringing tentacles
hypertrophies so that the entire gape can be
covered and appropriate openings locally
created for the inflowing current and the ex-
trusion of both exhalant current and of pseu-
dofaeces. The latter are of major significance
in pleurothetic species owing to the special
need to remove waste from the depth of the
mantle cavity on the under side. In the
Pectinacea, unlike the Pteriacea, pseudo-
faeces collect at both ends of the mantle
cavity at the base of auricles where their ex-
pulsion, with mantle margins locally separat-
ing, provides the backward “jet” responsible
for swimming—as distinct from escape—
movements in free living scallops. These ex-
pulsions are due to sudden contractions by the
Striated (quick) component in the adductor.
This is especially large in pectinaceans, par-
ticularly in those that swim. Its oblique orien-
tation in relation to the valves appears as an
adaptation which assists the closure of the
valves and so more efficient ejection (Thayer,
1972).

The reduced foot, initially solely concerned
with byssal formation (as in the Pteriacea)
retains the left posterior retractor needed for
pulling the animal down on the byssal attach-
ment. Where the byssus is lost (both in free-
dom and where cemented) the terminal pedal
cone may be enlarged to act as a cleansing
organ (as it is also in the Anomiacea) while the
pedal retractor atrophies. The foot is never
lost.

More complete reorganization of the vis-
ceral organs around the central adductor has
been accompanied by enlargement of the
visceral ganglia and reduction and posterior
migration of the cerebro-pleural ganglia.
These come close to the pedals in Pecten but
unite with the viscerals in Spondylus (Dakin,
1928a; Watson, 1930). This is in marked con-
trast to the unmodified condition noted in the
Pteriacea.

There remain for discussion two structures,
completely characteristic of the Pectinacea
yet both absent in the one family Propeamus-
sidae, namely the lip apparatus and the pallial
eyes. The former consists of arborescent
growths, two from the upper, and three from
the lower, lip which intimately interlock without
fusing to form a finely perforated tube cover-
ing the mouth and proximal oral grooves be-
tween these and the labial palps (Pelseneer,
1931). The apparatus in Pecten maximus is
described in great detail by Gilmour (1964)
while Bernard (1972) has reviewed the oc-
currence of such lip hypertrophy throughout
the Bivalvia. It is confined to the Pectinidae,
Spondylidae and the unrelated Limidae.
Clearly important because of its high elabora-
tion, there are varying views as to its function,
the lip apparatus appears to be associated
with the presence of an anterior rejection
area. This is so near the mouth that food
streams would tend to be carried away within
it if these were not confined within tubes that
allow only water to escape (Yonge, 1967).
Gilmour (1964) suggests a possible correla-
tion with the “anisomyarian” monomyarian
condition, but there is no lip apparatus in the
equally monomyarian Anomiacea (Yonge,
1977b).

The highly organized pallial eyes (Dakin,
1910) are situated usually among long sen-
sory tentacles on the middle fold of the mantle
margin, conspicuous glistening spots against
the often deeply pigmented inner mantle
folds. They occur in more or less equal num-
bers on both mantle lobes and are just as
numerous and well developed in the attached
Pedum, Hemipecten and Hinnites and in the
Spondylidae (Dakin, 1928b) as they are in the
swimming scallops. The contention is not
that they evolved in direct connexion with
swimming as is often assumed but at a far
earlier stage when the animals were byssally
attached and in association with the wide
gape and extensively exposed pallial tissues.
This still applies to all attached species. Ca-
pable of being stimulated by a passing or ap-
proaching shadow, these eyes would detect
the presence of a predator and initiate a reflex
response involving sudden closure of the
valves. Where the animals are free this in-
volves an “escape” reaction, water being ex-
pelled forward, and the animal making a sud-
den movement hinge foremost.

Consideration of adaptive radiation in the
Pectinacea must, therefore, start at a stage
before the Pectinidae evolved with the early
separation of the now abyssal Propeamus-

PECTINACEA AND HEMIPECTEN FORBESIANUS 27

siidae. There the shell (Waller, 1971, 1972,
1978) differs from that of the other Pectina-
cea, the right valve dominated by prismatic
calcite with crossed-lamellar aragonite pres-
ent in both valves and so resembling the
Palaeozoic Pernopectinidae of which they
may be the modern survivors. Adaptations in
this family will therefore be initially discussed
followed by those in byssally attached, free
and then cemented pectinids with the
Spondylidae, resembling the last considered
pectinid in habit, dealt with last of all. 2

ADAPTIVE RADIATION
Propeamussiidae Abbott, 1954 (Fig. 2b)

This family consists of deep-sea species
the habits of which can only be deduced.
Species of Propeamussium are free, but spe-
cies of Cyclopecten are byssally attached.
Personal examination has been made of the
four species of “Amussium” described by
Knudsen (1967) from the John Murray Expe-
dition and obtained from the British Museum

# PECTINIDAE N

PROPEAMUSSIIDAE

Лия
UN

ANOMIACEA

FREEDOM

BYSSAL ATTACHMENT

SPONDYLIDAE

CEMENTATION

FIG. 2. Adaptive radiation within the Pectinacea; drawings from above (left side) showing two regions of
adductor, foot with byssus and retractor (black), ctenidium and frilled lips (or open mouth); arrows as before. a,
Chlamys varia; b, Propeamussium sp.; с, Amusium, etc.; а, Pedum spondyloideum; e, Hemipecten
forbesianus; f, Hinnites multirugosus; д, Spondylus americanus; also (for comparison) h, Pododesmus sp.

(Anomiacea) (byssus obscured by retractor).

2The recently established family Syncyclonemidae Waller, containing both byssally attached and free Recent species, is

known only from the shell (Waller, 1978).

28 УОМСЕ

(Nat. Hist.). All are small with the maximum
dimension (height) between 15 and 50 mm,
the very delicate shell strengthened by inter-
nal radiating ribs. There is no byssal notch
and the valves are of similar external convex-
ity. Ligament and general body form are typi-
cally pectinacean but the ctenidia are simpler
being non-plicate and without interlamellar
junctions. There is a unique 6:1 ratio of stri-
ated to smooth muscle in the adductor and
the former is more obliquely disposed than in
other pectinaceans (Thayer, 1972). The foot
is without obvious terminal dilation but it may
distend with blood pressure and so could as-
sist in cleansing; it can have no other function.
Knudsen (1967) notes the presence of tenta-
cles and absence of eyes on the middle mar-
ginal fold and hypertrophy of the inner fold
(velum), and this is very pronounced in the
specimens personally examined (shown stip-
pled in Fig. 2b). Some species of Cyclo-
pecten (Knudsen, 1970; Bernard, 1978) have
a byssal notch, the small foot possessing a
byssal apparatus, the solitary left retractor
being divided. The ratio of striated to smooth
muscle is here some 3:1. There is the unique
presence of a strand of muscle overlying the
rectum and connected with a large abdominal
sense organ (Bernard, 1978).

There is every indication that Propeamus-
sium spp. are most highly efficient swimmers;
the habits of Cyclopecten with some spp. at-
tached are more difficult to deduce. From
identification of crustacean and other animal
remains in the stomach of species of Propea-
mussium Knudsen deduces a carnivorous
habit. This is supported by the extreme depth
of the inner mantle folds which indicates an
exceptionally wide gape, prey being possibly
entrapped during the swimming movements
and then held within the mantle cavity. Ab-
sence of a lip apparatus would enable small
animals to enter the mouth. The presence of
an anterior ejection current (necessary for the
forward and possibly “feeding” movements)
would not divert food of this size. There is no
corresponding evidence that Cyclopecten
species are carnivorous.

Pectinidae Rafinesque, 1815
Chlamys varia (Fig. 2a)
This species, fully pleurothetic but usually
byssally attached throughout life, a habit that

persists in a variety of pectinids, is taken as
representing the original mode of life in the

Pectinidae. The general characters have al-
ready been outlined, the shell rounded and the
valves with large auricles and, apart from the
byssal notch on the right, very similar in form
and convexity. A small left posterior pedal re-
tractor persists in functional association with
the attaching byssus. The ratio of quick to
catch muscle in the adductor is some 2.5:1, a
presumed adequate provision for the needs of
pseudofaecal extrusion.

Amusium, Pecten and Chlamys spp. (Fig. 2c)

After brief initial attachment, all species of
the two first genera become free and many,
such as C. opercularis in the last genus (al-
though C. septemradiatus remains attached
for two years (Allen, 1953)). Movement is by
jet-propulsion, its relation to muscular mech-
anics fully discussed for many pectinids by
Gould (1971), Moore & Trueman (1971) and
Thayer (1972). Conclusions that, apart from
possibly Propeamussium spp., the most ef-
ficient swimmers are species of the highly
streamlined Amusium with internally ribbed
very equivalve shell has now been demon-
strated in life by Morton (1980) for A. pleuro-
nectes which attains a speed of between 37
and 45 cm/sec. Necessary turning over of
these free pectinids if coming to lie on the left
is accomplished by localized overlapping of
the inner mantle folds and a “downward” ex-
pulsion of water. Pecten maximus and related
species are very inequivalve, with the right
valve deeply concave internally and the left
valve almost flat. They create cavities in a
usually sandy substrate and may seldom
swim although making efficient escape move-
ments if a predator, usually an echinoderm,
approaches. All these swimmers retain a very
small left posterior pedal retractor. The ratio of
striated to smooth muscle is some 3:1 in C.
opercularis and P. maximus but increases to
5:1 in Amusium. The ubiquity and great abun-
dance of unattached scallops indicates the
success of this epifaunal and mobile mode of
life.

Pedum spondyloideum (Fig. 2d)

Here adaptation involves retention of
byssal attachment but to a specific substrate,
namely the living surface of a scleractinian
coral that reacts by its growth to the presence
of the bivalve (Yonge, 1967). This solitary
species of the genus which occurs usually
(perhaps always) on species of Porites was

PECTINACEA AND HEMIPECTEN FORBESIANAUS 29

originally described and figured in situ by
Quoy & Gaimard (1830-35) in their account of
the zoology of the voyage of the Astrolabe.
Living individuals were personally studied at
Rabaul, New Britain, during the cruise of the
Stanford University Research Vessel Te Vega
in February 1965.

The veliger larva must metamorphose ex-
clusively on the living coral surface to make
permanent byssal attachment with the free
margins of the valves pointed upward. It so
influences the growth of the coral that the
elongate pectinid comes to live in deep clefts
in which the heavily pigmented inner mantle
lobes with the glistening eyes are highly con-
spicuous when the valves open. There is a
large byssal notch, only exceeded by that in
Hemipecten. The foot is exclusively con-
cerned with secretion and planting of the large
byssus which involves hypertrophy of the left
posterior pedal retractor, the contraction of
which draws the animal downward in the cleft
when the adductor also contracts. Owing to
the necessary upward growth which prevents
overgrowth by the coral, there is a consider-
able ventral (upward) migration of the hinge
line, a condition otherwise only present in the
cemented species. There is some movement
(near to the opening above) of the posterior
pseudofaecal accumulation but the anterior
accumulation continues to be situated near
the mouth which is protected by the lip ap-
paratus. For better food collection within the
enclosing cleft, the posterior tips of the
ctenidia extend beyond the confines of the
shell to be withdrawn by enlarged branchial
muscles. The ratio of striated to smooth mus-
cle in the adductor is much as in Chlamys
varia indicating a corresponding need for
pseudofaecal extrusion.

This is a very specific instance of adapta-
tion with the living substrate reacting to pro-
vide a very secure habitat to the elongate
pectinid.

Hemipecten forbesianus (Figs. 2e, 3-5)

The most intimate development of byssal
attachment occurs in this widely distributed
species. With the type-locality in the Sulu
Archipelago, living specimens were person-
ally examined in January 1978 after they had
been collected off Dunsborough, some 200
miles S of Perth, Western Australia, by Dr.
Barry Wilson then of the Western Australian
Museum. Later preserved specimens with
drawings and photographs were received

0.5 ст

FIG. 3. Hemipecten forbesianus, right (under)
valve showing circular form and depth of byssal
notch.

from Mrs. S. M. Slack-Smith, Curator of the
Mollusc Department in that Museum, who will
be producing a general description of this
species including ecology and distribution.

The specimens originally collected were at-
tached to the smooth under surface of colo-
nies of the scleractinian coral, Turbinaria
mesenterina (Dana) which grow in the form of
stalked cake baskets with the large polyps
rising exclusively from the upper surfaces.
The extremely compressed and almost com-
pletely circular pectinids were up to 2 cm in
diameter, the upper valves reddish brown and
rough, usually with epiphytic growths, the
lower valves extremely thin and completely
smooth. They conform perfectly to the coral
surface against which they are adpressed.
The byssal notch is extremely deep, curving
inward towards the umbo (Fig. 3). The mas-
sive byssus extends through it in an obliquely
upward (dorsal) direction (Figs. 4, 5). The
stout threads appear to be calcified terminally
but this may be due to adherence of frag-
ments of coral skeleton.

As noted by Adams & Reeve (1850) in their
original description of this species, “this inter-
esting shell is intermediate in its characters
between Pecten and Anomia” with “a sinus
so deeply cut in the direction of the hinge-
margin as to remind one of Pedum.” Actually,
as already noted, the notch is much less deep
in that pectinid. In the one previous descrip-
tion of the animal of H. forbesianus—a soli-
tary specimen obtained during the Siboga

30 YONGE

WY
W

NO
М

N к
WS

aur

Ц
= ТР

TT]

AAA
0.2 ст

FIG. 4. Н. forbesianus, animal viewed from right side after removal of right valve and greater part of right

mantle lobe.

Expedition—Pelseneer (1911) refers to vari-
ous earlier views stressing these intermediate
characters but concludes that this is an un-
doubted pectinid. Interest resides in the ex-
treme intimacy of byssal attachment. This in-
volves the deep byssal notch with the hyper-
trophied byssal apparatus (Figs. 3, 4) which
has been pushed far forward on the right side.
This produces asymmetry at the anterior end,
the left palps lying above the right palps and
the small pedal tip (f) displaced to the left side
(Fig. 5). There is some asymmetry also in the
heart and pericardium. The mantle margins
are richly supplied with eyes but the inner
marginal fold with fringing tentacles is of only
moderate size: both sides of the pallial notch
in the region where the byssus extends bear
numerous tentacles. Probably the valves do
not gape widely when adductor and pedal re-

tractor relax. The homorhabdic ctenidia have
12 rows of ciliary junctions in the descending
lamellae but only six on the much shorter
ascending limb. There is no evidence that the
ctenidia extend beyond the shell margins as
they do in Pedum. The small mouth is guard-
ed by frilled lips. This was noted by Pelseneer
(1911) who also observed the absence of a
right anterior pedal retractor and the immense
hypertrophy of the left retractor where condi-
tions do approach those in the Anomiacea (cf.
Figs. 2e & h). The two portions of the smaller
adductor are separate with the smooth part
only a little the smaller. Owing to the posture
of the animal, prolonged adduction must be
as important as cleansing contractions.

H. forbesianus resembles P. spondyloid-
eum in being the sole species in the genus,
being permanently attached by byssus

PECTINACEA AND HEMIPECTEN FORBESIANAUS 31

ааа

FIG. 5. H. forbesianus, animal viewed from left side after removal of valve; only eyes indicated on mantle

margins.

threads and apparently always to scleractin-
ian corals although without affecting their
growth. in both, the larvae must settle by pref-
erence on the living surface of appropriate
corals. The mode of attachment is more spe-
cialized in Hemipecten, resembling the
Anomiacea with the byssus emerging more or
less centrally but in the former directed dor-
sally instead of laterally (i.e. topographically
downward) and so without the same separa-
tion of the anterior region of the ctenidia (Fig.
2h) with the palps. In Hemipecten hyper-
trophy of the byssal apparatus is associated
with atrophy of the terminal regions of the foot
unlike the Anomiacea where this extends as a
potent cleansing organ and is so retained in
Placuna where the byssus apparatus is lost
(Yonge, 1977b).

Hinnites multirugosus (Fig. 2f)

Here settlement and metamorphosis are
followed by a period of freedom, the animals
behaving like other scallops, swimming by jet
propulsion with periods of temporary byssal
attachment. In the Californian H. multi-
rugosus, common on rocks to depths of 60 m,
to which knowledge of the living animal is

largely confined (Yonge, 1951) cementation
occurs at diameters of between 2.2 and
4.2 cm. This is easily determined by examina-
tion of the under valve, the surface being
regular prior to attachment and then conform-
ing to an irregular rocky substrate, the upper
valve becoming correspondingly irregular. As
described elsewhere (Yonge, 1979), cemen-
tation involves a change in the physical prop-
erties of the periostracum which comes from
the groove on the inner side of the outer mar-
ginal fold on the right mantle lobe. At this
stage in growth this must alter physically so
as to adhere to the substrate, the prismatic
layer secreted by the outer surface of the
outer fold attaching to this and so also the
inner calcareous layer formed by the outer
mantle surface.

The rounded pectinid form is initially little
affected, the most striking difference, due to
attachment (as in Pedum), being the hinge line
which is displaced ventrally with accompany-
ing loss of the auricles. Large specimens
reach lengths, hinge to free margin, of 20 cm.
The ligament is normal, its previous stages
apparent on the exposed dorsal area of the
right valve. The sites of pseudofaecal extru-
sion move somewhat ventrally but the lip ap-

32 YONGE

paratus is retained. After attachment the
byssal apparatus atrophies and the foot per-
sists as a cleansing organ although it is less
modified for that purpose than in Pecten. The
inner mantle folds are deep, some 1.5 cm in
an animal 8 cm in diameter, fringed with small
tentacles and deep orange in colour with
black pigment internally. The middle fold
bears long tentacles and conspicuous eyes.
The ratio of striated to smooth muscle in the
adductor is an unexpected 4:1 but the shell is
much thicker and so heavier than in byssally
attached or free pectinids and so may require
great force for sudden ejection but owing to
the weight of the free valve have less need for
the means of continued closure.

Spondylidae Gray, 1820
Spondylus americanus (Fig. 2g)

This family comprises large and conspicu-
ous members of the associated fauna of coral
reefs, this species alone in the Caribbean, but
many species in the Indo-Pacific. The thick
left valve is often richly coloured and bears
characteristic spines. Internally both valves
are concave, the right one deeper. The shell
is even more inequivalve than in Hinnites, the
dorsal hinge region of the right valve elongate
and curved representing change in the hinge
line during growth. Cementation occurs very
early, apparently immediately after prior
byssal attachment which is indicated by the
presence of а byssal notch in the postlarval
shell.

Knowledge of anatomy is based primarily
on the work of Dakin (1928a) on the Mediter-
ranean S. gaederopus and Yonge (1973) on
S. americanus which involved study in life.
The general form of the visceropedal mass is
very similar to that of the Pectinidae, unlike
the Propeamussidae; both lip apparatus and
pallial eyes are present. There are the same
anterior and posterior accumulations of
pseudofaeces, the ratio of striated to smooth
muscle in the adductor about 2:1, a difference
from conditions in Hinnites to be explained by
differences in the hinge. The foot becomes a
highly efficient cleansing organ (Yonge,
1973). There is a very interesting difference in
the nervous system with a much greater con-
centration of nerve ganglia in the visceral re-
gion than in the Pectinidae (Dakin, 1928a;
Watson, 1930; Pelseneer, 1931).

The major differences between the families
reside in the mantle/shell with major effects
on the hinge and ligament. Taylor, Kennedy &
Hall (1969) note significant differences in shell
structure. Although the hinge superficially re-
sembles that in the Pectinidae, the long lateral
regions are occupied by fused periostracum
not by outer ligament layer. The epithelia
secreting this have been displaced centrally
where their secretion is added to both sides
(i.e. topographically above and below) the in-
ner ligament layer. Formation of the second-
ary ball-and-socket hinge teeth is also as-
sociated with this downward invasion of the
fused mantle margins from both ends. There
are resemblances here to the Plicatulacea but
the visceropedal affinities with the Pectinacea
are undoubtedly of greater significance.

ACKNOWLEDGEMENTS

Thanks are initially due to Dr. Barry Wilson
and Mrs. Shirley Slack-Smith both then of the
Western Australian Museum, Perth, for intro-
duction to Hemipecten forbesianus in West-
ern Australian waters, then to Dr. J. E. N.
Veron of the Australian Institute of Marine
Science, near Townsville for his identification
of the coral to which this pectinid attaches it-
self, to the British Museum (Nat. Hist.) by way
of Dr. John Taylor for the supply of various
species, notably of the Propeamussiidae. Mr.
J. J. Holmes, Departmental Superintendent
gave great assistance in the preparation of
figures. | have finally to thank Prof. J. M.
Mitchison, F.R.S., for facilities in his Depart-
ment, my wife for technical and typing help
and the Natural Environment Research
Council for the assistance provided by Grant
GR3/1380.

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MALACOLOGIA, 1981, 21(1-2): 35-60

THE ANOMALODESMATA

Brian Morton

Department of Zoology, University of Hong Kong, Pokfulam Road, Hong Kong

ABSTRACT

The bivalve subclass Anomalodesmata Dall, 1889 is globally distributed and characterized by
widely diverse species, both in form and habits, occupying extremely specialized, narrow, almost
exclusively marine niches.

The subclass possesses a single order—the Pholadomyoida Newell, 1965—and is generally
considered to comprise a number of extant superfamilies, though their definition is not univer-
sally agreed upon. More agreement has been reached with regard to the number of families—
higher taxa for which clearer definitions are available. Each family comprises but a few extant
genera and species.

The possession by most of a number of common characters, i.e. no hinge teeth, a ligamental
lithodesma, gill structure of type E, the presence of a fourth pallial aperture, extensive mantle
fusion and simultaneous hermaphroditism, indicates that the subclass arose from a pholado-
myacean stock in the early Palaeozoic. A few representatives of the Pholadomyacae survive
today and it is from a study of these that present views on the phylogeny of the Anomalodesmata
have been derived. In the Palaeozoic, the Pterioida were the dominant colonizers of hard intertidal
and shallow sublittoral surfaces and generally exploiting the epi- and endobyssate modes of life.
They are still widely dominant in this habitat today.

The Anomalodesmata, with the Trigoniacea, were thus largely infaunal and enjoyed a brief
expansion, widely diversifying and adopting shallow and deep burrowing modes of life. There-
after, in the Mesozoic, the Anomalodesmata reveal a pattern of declining importance (in relation
to the period of expansion that will occur in the Caenozoic) but one superfamily—the Thraciacea
(herein defined) survived in specialized habitats. The decline in importance of the Anomalodes-
mata at this time possibly reflects the increasing importance of the evolving heterodont
Veneroida which then and now have come to dominate most ‘generalist’ infaunal, marine and
estuarine habitats—even coming to colonize fresh waters. The Anomalodesmata, it is here
argued, produced two further lineages, leading ultimately to the modern Poromyacea, Verti-
cordiacea and Cuspidariacea, which have thrived in deep waters and convergently came to
adopt macrophagous feeding habits. By modern standards these are the most successful
anomalodesmatans, accounting for a significant component of abyssal faunas.

In the Caenozoic, the Anomalodesmata have enjoyed a further expansion to produce the
Pandoracea and the Clavagellacea, both of which are primitively infaunal but have subsequently
radiated onto hard environments by the adoption of byssally attached and cemented modes of
life.

Anomalodesmatan attempts at diversification have largely failed in competition with more
‘generalist’ bivalves (especially with regard to their simpler reproductive strategies) and the living
remnants of this, at times, numerous subclass remain today like the widely spaced outermost
twigs of a tree, the roots of which have long since perished and the trunk, represented today by a
few representatives of the Pholadomyacea, reduced to some of the rarest molluscs. Conversely,
however, they are wonderfully equipped to survive in specialized niches.

This paper reviews the main branches of anomalodesmatan evolution and attempts to show
how apparently irreconcilable morphological differences are but widely diverse expressions of a
unifying theme. Recent studies of extant pholadomyaceans have provided clues to an under-
standing of the Anomalodesmata in general but more importantly to the origin of the Clavagel-
lacea and the Poromyacea, Verticordiacea and Cuspidariacea—groups for which there were
hitherto no recognized phylogenetic backgrounds.

INTRODUCTION toral and deep water bivalves, occupying ex-

tremely narrow niches and exploiting a wide

The subclass Anomalodesmata Dall, 1889 variety of life styles. Only a single species of

with only one order—the Pholadomyoida the Lyonsiidae—Guianadesma sinuosum—is
Newell, 1965—is represented today by a di- fresh water (Morrison, 1943).

verse assemblage of marine, littoral, sub-lit- Although а few, e.g. members of the

(35)

36 MORTON

Lyonsiidae, i.e. Lyonsia and Entodesma
(Yonge, 1952; Narchi, 1968; Morgan & Allen,
1976), are byssally attached and others are
cemented, e.g. members of the Clavagelli-
dae, Cleidothaeridae and Myochamidae, i.e.
Clavagella, Cleidothaerus and Myochama
(Soliman, 1971; Morton, 1974; Yonge &
Morton, 1980), the vast majority are infaunal.
The burrowing species can be divided into
two major categories. Members of the
Poromyacea (i.e. including the three families
Verticordiidae, Cuspidariidae and Poro-
myidae) (as defined by Newell, 1969) are
abyssal whereas members of the Clava-
gellacea, Pandoracea and “Thraciacea”! live
in shallow waters. Two extant members of the
otherwise extinct and ancient superfamily
Pholadomyacea are equally — divided,
Pholadomya candida occupying shallow
waters (Morton, 1980a), species of Parilimya
living in deep waters (Morton, in prep.).

Within the deep water anomalodesmatans
there is a general trend towards a scavenging
and carnivorous mode of life (Yonge, 1928;
Reid & Reid, 1974; Allen & Turner, 1974; Allen
& Morgan, in press). The Poromyacea has
variously been considered to be mono- and
polyphyletic. Pelseneer (1888a,b, 1891, 1911)
and Allen & Morgan (in press) believe the se-
quence Verticordiidae-Cuspidariidae-Poro-
myidae to constitute a natural progression of
increasing specialization. Bernard (1974),
however, and, earlier, Dall (1890) and Plate
(1897) argued a diphyletic origin for the Poro-
myacea, indicating that the Verticordiidae and
the Cuspidariidae are more properly derived
from a lyonsiid-like ancestor, while the Poro-
myidae, with an external ligament, have a sep-
arate, older origin. The adoption of the carnivo-
rous habit in the Cuspidariidae and Poro-
myidae would thus represent convergent evo-
lution (Yonge & Morton, 1980). Bernard (1979)
subsequently modified his views somewhat
and located only the Verticordiidae (and resur-
rected family Lyonsiellidae G. Sars, 1871) in
the Pholadomyoida, placing the Poromyacea
and the Cuspidariacea in a separate order, the
Septibranchoidea.

The Pandoracea are a recent, Caenozoic,
assemblage and much easier to understand
because of a generally similar life style. They
can be derived from a lyonsiid ancestor
(Yonge & Morton, 1980), with a sunken pri-
mary ligament, invariably a ventral lithodesma

and tending towards distinct valve inequality.

As noted earlier, the families Thraciidae,
Periplomatidae and Laternulidae have tradi-
tionally been located in the Pandoracea
(Newell, 1965, 1969) but, it will later be as-
serted, they should be relocated in a separate
superfamily—the Thraciacea Stoliczka, 1870.
In these bivalves the primary ligament is lo-
cated between deep chondrophores, the shell
is thin and the lithodesma, where present, is
V-shaped, located on the anterior face of the
ligament, and constitutes an additional means
of valve alignment which is clearly not always
essential in some representatives of these
families.

The Clavagellacea are possibly the
strangest of all anomalodesmatans with a tiny
bivalve shell and an enormous tube-like ad-
ventitious shell and with an exchange of water
via the expanded “watering pot” plate around
the pedal gape, at least in Brechites
(Purchon, 1956a, 1960).

The ancient superfamily Pholadomyacea is
represented today by a number of exception-
ally rare genera, including Pholadomya
and Parilimya (Morton, 1980a, in prep.).
Though specialized, these bivalves fore-
shadow conditions in the more recent, extant,
anomalodesmatans and it has been from a
study of these bivalves that a better under-
standing of the Anomalodesmata has been
obtained—the adaptive radiation of which is
the subject of this paper.

PANDORACEA Rafinesque, 1815 (compris-
ing the Lyonsiidae Fischer, 1887, Pandoridae
Rafinesque, 1815, Myochamidae Bronn,
1862 and Cleidothaeridae Hedley, 1918)

Most studies of the Anomalodesmata have
concerned themselves with the Pandoracea.
The constituent families arose in the
Caenozoic. The oldest extant pandoraceans
are the Lyonsiidae and Yonge & Morton
(1980) consider this family to be the most
primitive especially in terms of ligament struc-
ture. By and large also, the Lyonsiidae (Fig. 1)
exhibit a relatively simple plan, being only
slightly inequivalve, with a typical ctenidium of
type E ciliation, protruding siphons with sen-
sory tentacles, extensive mantle fusions and
a fourth pallial aperture. Lyonsia norvegica is
infaunally buried (Ansell, 1967) but pos-

TFor а variety of reasons, Yonge & Morton (1980) have suggested that members of the Thraciidae, Periplomatidae and
Laternulidae should be separated from the other families of the Pandoracea as defined by Newell (1965, 1969).

THE ANOMALODESMATA

Fused
periostracum -——

Anterior outer
ligament layer

Inner ligament layer
/
< АА
> MAS

Lithodesma

NIE aa ERS SS >
ААА

Posterior outer

2mm
ligament layer

Lithodesma

FIG. 1. The Lyonsiidae. (A), Lyonsia norvegica in its natural position in sand (redrawn after Ansell, 1967);
(B), Entodesma saxicola (redrawn after Yonge, 1952); (C), (D), the ligament of E. saxicola, as seen from the
ventral and lateral aspects respectively (redrawn after Yonge, 1976).

sesses a tiny byssus. Most other lyonsiids are
strongly epibyssate e.g. Entodesma (Yonge,
1952), and are thus typically weakly hetero-
myarian in form and occupy crevices on rocky
shores. Mytilimeria inhabits the tunics of
tunicates (Yonge, 1952).

The Pandoridae (Fig. 2) have been studied
by Allen (1954, 1961a), Allen & Allen (1955)
and Boss & Merrill (1965). In this family there
is a marked valve inequality, the right flat, the
left convex. The shell is rounded ventrally and
peaked dorsally, the primary ligament, with a
long lithodesma, being sunken and located
between shallow resilifers. The shell pos-
sesses ‘secondary’ hinge teeth (Yonge &
Morton, 1980). Pandora inaequivalvis lies on
the convex left valve, buried in sheltered
sands at an angle of 40° to the surface (Allen
& Allen, 1955).

The Myochamidae (Fig. 3) comprise two
genera. Of these Myadora is the mirror image
of Pandora, the left valve flat, the right con-

vex. It occupies a similar ecological niche in
the Indo-Pacific as Pandora does in the Atlan-
tic, and also lies buried in the sand on the left,
but flattened, valve. Myadora striata inhabits
high energy beaches in New Zealand (Mor-
ton, 1977). In the second genus of the Myo-
chamidae—Myochama—the potential advan-
tages of valve inequality are first realised and
the animal is cemented by the right valve to
the protruding posterior borders of the shell of
shallow sublittoral bivalves (Yonge & Morton,
1980). The ornament of Myochama mimics
that of the host. Unlike members of the
Chamidae (Yonge, 1967) and Cleidothaeri-
dae (Morton, 1974), however, there is no
tangential growth component and in many
respects Myochama is but a cemented
Myadora. The dorsal region of the right valve
is not cemented to the substratum so that
there is no inequality to the ligament or the
ventral lithodesma. Similarly left and right
organs of the mantle cavity are of equal size.

38 MORTON

Anterior outer Posterior outer

Right Left

Inner

ligament layer ligament layer ligament

layer

Fused
periostracum

FIG. 2. The Pandoridae. (A), Pandora inaequivalvis in its natural position in the sand (redrawn from Allen,
1954 and Allen & Allen, 1955); (B), (C), the shell of P. inaequivalvis as seen from the anterior and the
structure of the ligament as seen from the left (redrawn after Yonge & Morton, 1980).

The siphons are separate and there is a fourth
pallial aperture.

The full effects of this general trend within
the superfamily towards increasing valve in-
equality are seen in the single genus—
Cleidothaerus—of the Cleidothaeridae (Fig.
4). The animal is attached by the right valve
which forms a deep cup, the left valve being a
flat disc. This marked valve inequality results
from the adoption of a cemented habit and is
accompanied by a tangential component to
growth not seen in other pandoraceans. Be-
cause of this component, the secondary liga-
ment of fused periostracum is split anteriorly
and the umbones separated, while the pri-
mary, sunken ligament largely comprises in-
ner ligament layer, is inequilateral and the
lithodesma appears to coil around it (Yonge &
Morton, 1980). The valve inequality is also re-
flected in the organs of the mantle cavity,
those of the left being smaller than those of
the right (Morton, 1974). As noted by Yonge
(1967) for the Chamidae, inequality only af-
fects the organs of the mantle cavity and not
the visceral mass (Morton, 1974).

The Pandoracea are best seen as relatively
modern descendants of a pholadomyacean
stock, that through valve inequality have
evolved a wide range of morphological spe-
cialisations and have successfully colonized
restricted niches in the lower intertidal and the
sublittoral, characteristically either lying on
one or other valve, rarely vertically, or ce-
mented by one valve. The Lyonsiidae are the
only known, extant anomalodesmatans with
a well developed byssus. in all cases these
adaptations allow occupation of high (wave)
energy environments. Other modifications
appropriate to such niches include rapid re-
burial in some (e.g. Myadora), but not others
(Pandora); large labial palps and efficient re-
jectory currents in the mantle cavity for the
removal of sediment and extremely sensitive
siphons quickly withdrawn between slightly
gaping valve margins.

Runnegar (1974) has accepted the views of
Pelseneer (1888a, b) of a continuous mor-
phological transition from a lyonsiid to a septi-
branch (i.e. the Poromyidae and Cuspidari-
idae) via a verticordiid and thus places the

THE ANOMALODESMATA 39

Anterior outer
C ligament layer

inner
ligament
layer

Lithodesma

“GY

Right Left

Posterior outer
ligament layer

_ inner
ligament

layer
/D
»

Ul]

5mm

FIG. 3. The Myochamidae. (A), Myadora striata in its natural position in the sand (redrawn after Morton,
1977); (B), (C), the shell of M. striata as seen from the anterior and the structure of the ligament as seen from

the left (redrawn after Yonge & Morton, 1980).

Verticordiidae, typically located within the
Poromyacea (Newell, 1965, 1969) in the
Pandoracea. Certain morphological features
are possessed in common but the most re-
cent study of the Verticordiidae by Allen &
Turner (1974) indicates that they are well
placed within the Poromyacea (as defined by
Newell, 1969). This will be further discussed.

THRACIACEA Stoliczka, 1870 (comprising
the Thraciidae Stoliczka, 1870, Periplomat-
idae Dall, 1895 and Laternulidae Hedley,
1918)

The Thraciacea form a natural assemblage
of three families—the Thraciidae, Periplomat-
idae and the Laternulidae and it is here for-
mally proposed following earlier statements
(Yonge & Morton, 1980), that this be recog-
nised in the classification of the Anomalo-
desmata. As pointed out by Boss (1978), the
members of this superfamily arose in the
Jurassic, whereas the other families of the

Pandoracea (previously described) and to
which they were earlier linked (Newell, 1965,
1969; Runnegar, 1974) arose in the Caeno-
zoic. This division of the superfamily Pan-
doracea is strongly supported, indeed was
originally given substance by the researches
of Boss (1978) and Yonge & Morton (1980)
the latter investigating the structure of the
primary ligament, a feature of high taxonomic
value (Yonge, 1978).

The Thraciidae (Fig. 5) are insufficiently
studied though Allen (1961b) has described
the shell morphology of the British species
and attempted an understanding of the liga-
ment of Thracia villosiuscula, this, apparently,
being essentially similar to that of Cochlo-
desma (Periplomatidae) with an anterior
lithodesma linking two chondrophores and a
primary ligament composed largely of inner
ligament layer (Allen, 1961b, fig. 2C). How-
ever, | have examined Thracia phaseolina
and 7. villosiuscula and found them to pos-
sess an external primary ligament with a very

40 MORTON

A B

Posterior

FIG. 4. The Cleidothaeridae. (A), Cleidothaerus maorianus as seen from the left anterior aspect and (B) an
internal view of the right shell valve showing the effect of the tangential component of growth upon the
orientation of the body (redrawn after Morton, 1974); (C), a dorsal view of the primary ligament almost
exclusively comprising inner ligament layer with the lithodesma coiled around it (redrawn after Yonge &
Morton, 1980).

Fused periostracum

Posterior outer ne External
ligament layer Resilifer ligament
Fused

periostracum

Lithodesma
Resilifer Inner ligament
layer

Lithodesma

1-5 mm

FIG. 5. The Thraciidae. Thracia villosiuscula. (A), The shell as seen from the right and (В), the ligament as
also seen from the right; (C), the ventral view of the ligament of T. phaseolina.

THE ANOMALODESMATA 41

weakly defined amorphous lithodesma.
Clearly Allen was actually examining Cochlo-
desma praetenue and not Thracia villosiu-
scula.

Members of the Thraciidae are approxi-
mately equivalve, with exceptionally thin shell
valves; there is no obvious transverse crack in
the shell as there is in members of the
Periplomatidae and Laternulidae. The animal
typically lies vertically disposed in sandy de-
posits. The foot is large and the pedal gape
extensive. There are separate siphons (with
long siphonal retractors) which are pushed
upwards and form mucus-lined tubes with
separate siphonal holes in the sand (Yonge,
1937) as also occurs in Offadesma angasi
(Periplomatidae) (Morton, 1981).

Chondrophore

Inner
ligament

layer

2mm

Members of the Periplomatidae (Fig. 6)
have been investigated by Pelseneer (1911)
(Asthenothaerus), Allen (1958, 1960) (Coch-
lodesma) and more recently by Morton (1981)
(Periploma (Offadesma) angasi). In these
bivalves there is ап inequivalve shell,
this being of less significance in Cochlo-
desma but of greater importance in Offa-
desma. The primary ligament, largely com-
prising inner ligament layer, is internal and
located between spoon-shaped chondro-
phores. Cochlodesma praetenue does (Allen,
1958, 1960) but Offadesma angasi does not
(Morton, 1981) possess an anterior litho-
desma. The dorsal margin of the shell valves
are strongly united by periostracum forming a
secondary ligament. Of much greater impor-

FIG. 6. The Periplomatidae. (A), Offadesma angasi in its natural position in the sand (redrawn after Morton,
1981); (В), anterior view of the ligament of Cochlodesma praetenue; medial section through the ligament of
(С), a hypothetical ancestor; (D), Cochlodesma praetenue; (E), Offadesma angasi. (В, С, and D redrawn after

Yonge & Morton, 1980).

42 MORTON

tance in the Laternulidae, the Periplomatidae
(but not obviously the Thraciidae) possess a
transverse umbonal crack in each valve. This
is formed as the result of a trend in the super-
family for the antero-dorsal region of the shell
to overarch the postero-dorsal border, result-
ing also in the ligament swinging downwards
(for different reasons a similar ligament is
seen in the Cuspidariidae (Yonge & Morton,
1980)). Typically the thin valves gape both
anteriorly and posteriorly and Offadesma
angasi lies buried on its left valve some
6 cm below the surface in sub-littoral fringe
sands of high (wave) energy beaches. Sepa-
rate siphons, very similar to those of Thracia
(Yonge, 1937), project up to the water above.
Offadesma cannot rebury itself, the foot and
pedal gape being small unlike those of
Thracia which are large. The ctenidia are
large, the palps long and there are extensive
pallial glands to aid the discharge of the large
amounts of material that must enter the man-
tle cavity.

The Laternulidae (Fig. 7) are the most un-
usual and the most advanced family of the
Thraciacea. Indo-Pacific in distribution (Mor-
ton, 1976a), they possess a thin, approxi-
mately equivalve shell and lie more or less
vertically disposed in soft sediments ranging
from tropical mangrove muds (Laternula
truncata) (Morton, 1973), to the Antarctic
benthos (L. elliptica) (Burne, 1920). There are
always wide anterior and posterior gapes and
the exchange of mantle fluids is by anterior
and posterior adduction and thus flexion of
the valves at the transverse umbonal crack
against the fulcrum provided by the primary
ligament and the ventral shell margin (Morton,
1976a). A buttress, only weakly developed in
the Thraciidae but somewhat more robust in
the Periplomatidae, is strongly developed in
these bivalves and prevents breaking of the
valves under the forces generated by the ad-
ductor muscles. A boomerang-shaped
lithodesma occurs on the anterior face of the
primary ligament of some (e.g. L. truncata
and L. boschasina) but not other (L. elliptica,
L. anatina, L. anserifera) species (Morton,
1976a) and aids, in the absence of hinge
teeth, the secondary ligament of periostracum
in valve alignment.

The siphons of L. truncata are fused to the
tips and, unlike any of the families earlier de-
scribed, all of which possess simple sensory
papillae, the siphonal orifices are surrounded
by a complex array of sensory tentacles and
by nine pallial eyes with a complexity of struc-

A Lithodesma

ря

Chondrophore

Posterior
adductor Orbital
muscle muscle
|

RESULTANT
® REACTION
\

Transverse
crack in _
shell

RESULTANT |
REACTION |

Anterior
adductor
muscle

FIG. 7. The Laternulidae. Laternula truncata. (A),
anterior view of the ligament (redrawn after Morton,
1973); (B) and (C) the mode of operation of the
shell (redrawn after Morton, 1976a).

ture similar to that seen in the Pectinidae
(Adal & Morton, 1973) and more reminiscent
of vertebrate optical structures. In most re-
spects the organs of the mantle cavity and
visceral mass are, however, similar to those
of other families of the Thraciacea. Indeed
this generalization can be broadened to in-
clude members of all families of the Pan-
doracea and the relatively uniform nature of
the organs of the mantle cavity does not ap-
proach the complexity seen in other members
of the remaining anomalodesmatan lineages.

CLAVAGELLACEA d'Orbigny, 1844 (com-
prising only the Clavagellidae d'Orbigny,
1843)

The Clavagellacea (Fig. 8) are an enigma
with no recognized ancestor. They have

THE ANOMALODESMATA

Valves

Muse
ER

“watering pot”

Icm

Septal muscle

MOO N
ААА“

“Watering pot”

Pedal gape

FIG. 8. The Clavagellidae. The shell and adventitious shell of Penicillus sp. (redrawn after Taylor, Kennedy &
Hall, 1973); (В), (С), the shell and adventitious shell of two species of Clavagella (redrawn after Soliman,
1971); (D), Brechites penis. A dissection of the anterior end as seen from the right side (redrawn after

Purchon, 1960).

arisen relatively recently, the oldest fossils (of
Clavagella) being recorded from the Upper
Cretaceous. Brechites penis has been
studied alive by Purchon (1956a, 1960) and
Clavagella by Soliman (1971) though there
are earlier studies of, presumably, preserved
specimens by Owen (1835) and Lacaze-
Duthiers (1870). Smith (1971) has revised the
taxonomy of the group, dividing the living
representatives into the two genera noted
above, though Keen & Smith (1969) recog-
nise three genera, Clavagella, Humphreyia
and Penicillus. In Clavagella, one valve only
is fused to an adventitious shell while in
Brechites both valves are so fused. In both
genera the true shell valves are reduced to
small proportions in relation to the adventi-

tious shell which may be exceedingly large
and in Brechites (Purchon, 1956a, 1960)
forms a very long tube. Smith (1978) has
presented a few ideas on how the adventi-
tious shell is secreted. The anterior end of the
adventitious shell of Brechites is formed into a
“watering pot,” or expanded plate perforated
by many small pores. This end lies buried in
the sand and water is pumped in and out of it
by complex “septal” muscles around the
pedal gape (Purchon, 1956a, 1960).
Members of the Clavagellacea possess an
external ligament. Because of their immobile
way of life and reduced shell valves relative to
the adventitious shell the adductor muscles
are either very reduced or absent. Again,
however, typical ctenidia and labial palps are

44 MORTON

present and the organs of the visceral mass
seem unspecialized. Individual species, how-
ever, await detailed examination.

POROMYACEA Dall, 1886 (comprising the
Verticordiidae Stoliczka, 1871, Cuspidariidae
Dall, 1886 and Poromyidae Dall, 1886)

Altogether three families of deep water bi-
valves—the Verticordiidae, Cuspidariidae and
Poromyidae—are usually linked in a single su-
perfamily, the Poromyacea (Newell, 1965)
1969). Thus Pelseneer (1888a) and Ridewood
(1903) and, most recently, Allen & Turner
(1974) and Allen & Morgan (in press) recog-
nise a continuous morphological sequence—
Verticordiidae — Cuspidariidae-Poromyidae—
culminating, in the latter two families, in the
adoption of a carnivorous mode of life (Yonge,
1928; Reid & Reid, 1974). There are, however,
strong arguments against such a simplistic
view and the opinions of other authors (re-
viewed by Morton, in prep.) conflict with this.

À Posterior outer
Lithodesma ligament layer
| Fused
periostracum

Taenioid
muscle

К seems therefore appropriate to describe
each family in turn and later to discuss their
relationships one with the other and with the
other members of the Anomalodesmata.

The Verticordiidae (Figs. 9, 10) possess a
thin shell with a sunken primary ligament and
a ventral lithodesma. Ligament structure is
exactly as described for Lyonsia
(Pandoracea) (Yonge, 1976; Yonge &
Morton, 1980). The shell is also three layered
аз in members of the Pandoracea and
Thraciacea (Taylor, Kennedy & Hall, 1973).
Members of the Verticordiidae have been
extensively described by Allen & Turner
(1974). They are hermaphrodite and possess
a reduced ctenidium, of typical anomalo-
desmatan structure and labial palps formed
into a trumpet for the reception of large food
particles. They also possess—as in members
of the Pandoracea, e.g. Lyonsia (Prezant,
1979), and Thraciacea, e.g. Offadesma
(Morton, 1981)—well defined radial mantle
glands that serve to adhere sand grains to the

Right Left

FIG. 9. The Verticordiidae. Lyonsiella abyssicola. (A), (B), The ligament as seen from the right side and the
shell as seen from the dorsal aspect (redrawn after Yonge & Morton, 1980); (C), the tissues of Lyonsiella

fragilis (redrawn after Allen & Turner, 1974).

THE ANOMALODESMATA 45

periostracum. The siphonal tentacles are
complex, large and sticky and it is thought that
they form a fan of spreading papillate ad-
hesive structures which capture either dead
but possibly living organisms. In some verti-
cordiids the siphons are withdrawn by si-
phonal retractors (taenioid muscles), some of
which are longer and have separate points of
insertion upon the shell. In this feature
Lyonsiella fragilis (Allen and Turner, 1974)
most strongly resembles the pholadomyacean
Parilimya (Morton, in prep.).

The Cuspidariidae (Fig. 11) also possess a
thin shell and a sunken, opisthodetic primary
ligament with a lithodesma. The posterior
margin of the shell is typically rostrate. The
siphons, particularly the inhalant, are ex-
tremely long and raptorial, to be rapidly dis-
tended to catch living, mobile prey. Corre-
spondingly there are also numerous, large
sensory tentacles and accessory siphonal
ganglia (Reid & Reid, 1974; Reid & Crosby,
1980). The ctenidia are reduced to a hori-
zontally oriented septum perforated by pores
or ostia. The septum is used for prey capture,
the process involving the complex interaction
of a number of muscle blocks and hydrostatic
forces all designed to rapidly evert the in-
halant siphon. The structure of the septum
and the mode of operation of the organs of the
mantle cavity have been described by Yonge
(1928), Reid & Reid (1974), Reid & Crosby
(1970) and Allen & Morgan (in press).

Buccal mass

Lateral
lip

The Poromyidae (Fig. 12) differ from the
two previous families in one important char-
acteristic, the primary ligament is external and
does not possess a lithodesma (Yonge &
Morton, 1980). In many other respects the
Poromyidae closely recall conditions in the
Cuspidariidae, owing to the common pres-
ence of a septum, again for the capture of
living prey. The shell of the Poromyidae is not,
however, rostrate and clearly prey capture
must be by some other means, different from
that employed in the Cuspidariidae. Poromya
has siphonal appendages similar to those of
verticordiids (Yonge, 1928).

In both the Cuspidariidae and the Poro-
myidae the stomach is modified for the diges-
tion of large organisms (Yonge, 1928;
Bernard, 1974); in Cardiomya a digestive pro-
tease has been found (Reid, 1978).

PHOLADOMYACEA Gray, 1847 (Pholado-
myidae Gray, 1847)

Modern representatives of this ancient, old-
est lineage of the Anomalodesmata are
among the rarest bivalves. Hitherto the
Pholadomyacea have been considered to
comprise a single extant family—the Pholado-
myidae Gray, 1847, the type-genus and spe-
cies being Pholadomya candida Sowerby,
1823 (Morton, 1980a). Morton (in prep.), how-
ever, is erecting a second family—the Parili-
myidae Morton, 1981—following a detailed ex-

Oesophagus

Tongue

FIG. 10. The Verticordiidae. Lyonsiella formosa. (A), (B), Lateral views of the mouth region and the same in
longitudinal sagittal section (redrawn after Allen & Turner, 1974).

46 MORTON

Lateral
septal
muscle

dns
septa
A muscle

Posterior
adductor
muscle

Posterior
septal
muscle

Anterior
septal
muscle

Haemocoelic
lacunae

Anterior
septal
muscle

| +-—— adductor
ЧТ muscle

Foot

FIG. 11. The Cuspidariidae. (A), Cuspidaria rostrata, a decalcified specimen seen from the right. (B),
Transverse section through Cuspidaria sp.; (C), the septum, as seen from the ventral aspect, of Cuspidaria
cuspidata. (A, B, redrawn after Reid & Reid, 1974; C, redrawn after Yonge, 1928).

amination of Parilimya fragilis Grieg, 1920.
Other constituent genera of the new family
include Panacca and Nipponopanacca. All
are deep water bivalves.

In Pholadomya candida (Figs. 13, 14)—
probably the only living representative of the
genus—the ligament is external, there is no
lithodesma and the shell gapes widely both
anteriorly and especially posteriorly. The thick
siphons are fused almost to their tips with no
terminal sensory tentacles. Instead, a sensory
appendage—the opisthopodium—is located
on the posterior region of the visceral mass
and monitors water flow, supplying informa-
tion directly, and unusually, to the pedal
ganglia. In most anatomical respects Pholado-
mya is similar to other anomalodesmatans but
with one or two further notable exceptions.
The lips of the mouth (Fig. 14) are fused into
two, round, laterally positioned spheres which
probably serve, as in other bivalves in which
this occurs, e.g. members of the Pectinidae,
Spondylidae and Limidae (Morton, 1979), to
prevent food material from being flushed out
of the oral grooves by strong water currents in
the anterior region of the mantle cavity. The
second, major, modification involves the

pedal gape. From a point of attachment to
each shell valve outside the anterior adductor
muscle arises a thin muscle which crosses
over, anterior to the pedal gape, and has its
other insertion at the pallial line on the oppo-
site valve (Runnegar, 1979; Morton, 1980a).
These taenioid muscles have a structure remi-
niscent of the cruciform muscles of the
Tellinacea (Yonge, 1949). The foot is glandu-
lar, possesses two extravagantly complex
statocysts and is plug-like. It has been sug-
gested (Morton, 1980a), on the evidence of
the above adaptations, that P. candida lies
diagonally on its back in the sand and pumps
deposits into the mantle cavity via the pedal
gape, the foot acting as a piston with the
(mechanical) “valve” of the pedal gape and its
musculature. The gut is variously adapted for
dealing with large amounts of sediments.
Parilimya fragilis (Figs. 15, 16) is clearly
very different from Pholadomya; indeed,
Runnegar (1974) considered that it might be-
long to a different family, but linked to the
superfamily by the possession of an external
ligament, a distinctly radially ridged shell
which, however, does not gape or if so only
slightly and the common presence of taenioid

THE ANOMALODESMATA 47

A Anterior outer
ligament layer

Hinge tooth
N

Posterior outer

ligament layer
Inner
ligament
layer ~

Fused
periostracum —

Posterior
labial palp

sieve

Mouth

Anterior
labial palp

Imm Septum

Inne
Posterior outer
ligament layer ligament
layer

Fused
> periostracum

Anterior outer = as
ligament layer

\
\

SS Socket

Exhalant
D [| siphon

Inhalant
2mm siphon

FIG. 12. The Poromyidae. Right (A) and left (B) views of the hinge plate of Poromya tornata; (C), ventral view
of P. granulata with septum exposed and (D), the siphons of P. granulata (C and D redrawn after Yonge,

1928).

muscles. Members of this genus are more
numerous, there being a number of extant
species, all recorded from deep waters. In a
major revision of these bivalves, Morton (in
prep.) has placed Parilimya, Panacca and
Nipponopanacca т a new family—the
Parilimyidae—so different is the type-genus
Parilimya from Pholadomya—but neverthe-
less still included in the Pholadomyacea.
The organs of the mantle cavity of Parilimya
fragilis are typical of other anomalodes-
matans except with regard to the labial palps
and the siphons. In the latter case the inhalant
siphon is greatly elongate and muscularized
and can be withdrawn into the mantle cavity,
possibly rapidly, by two extraordinarily long
siphonal retractor muscles (one on each side)
and which find insertion on the shell towards
the anterior end of the mantle cavity. Similar
“taenioid” muscles, as noted earlier, occur,
albeit greatly reduced, in Pholadomya and in

Lyonsiella fragilis and possibly also Laevi-
cordia horrida in the Verticordiidae (Allen 8
Turner, 1974). The ctenidia are relatively
large. The labial palps (Fig. 16) are small,
muscular, with few sorting grooves. Structure
and interpreted function appear reminiscent
of the palps of the Poromyidae (Yonge, 1928)
and Verticordiidae (e.g. Lyonsiella formosa)
(Allen & Turner, 1974) ¡.e. for holding large
food items and certainly not for sorting fine
particles. Final evidence for a scavenging or
carnivorous mode of life in Parilimya comes
from an examination of the stomach and in-
testine which is modified, as in the Cuspi-
dariidae, Poromyidae and some members of
the Verticordiidae, i.e. stomach type Il
(Purchon, 1956b) for the digestion of large
pieces of food (Morton, in prep.).

The structure and interpreted modes of life
of Pholadomya and Parilimya gives valua-
ble insights into the evolution of two

48 MORTON

à
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A NZ 72238;
25cm
Anterior Via a
f= adductor С $ 4
muscle 4

puma na дик

ug”
>.

EN y

E |

ER \

4 —*__Haemocoel
da, ААА!
die, 50,

Pedal gape
muscle

25mm

FIG. 13. The Pholadomyidae. Pholadomya candida. (A), the animal in its interpreted position in the sand;

(B), exterior view of the pedal gape and musculature; (C), transverse section through the mantle (all redrawn
after Morton, 1980a).

other anomalodesmatan superfamilies—the PHYLOGENETIC LINEAGES
Clavagellacea and the Poromyacea (as de-
fined by Newell, 1969)—though again, study К is clear that the Pholadomyacea is the

of the Pholadomyacea casts further light on stem superfamily of the Anomalodesmata—
the evolution of the subclass as a whole. adaptive radiation proceeding in a number

THE ANOMALODESMATA 49

Anterior
adductor
muscle

Fused lips
of mouth

FIG. 14. The Pholadomyidae. Ventral view of the
fused lips and labial palps of Pholadomya candida
(redrawn after Morton, 1980a).

Taenioid sm

muscle

FIG. 15. The Parilimyidae. Parilimya fragilis as seen
from the right side after removal of the right shell
valve and mantle lobe (redrawn after Morton, in

prep.).

Anterior
labial pal
À ve P labial palp

Posterior
labial palp

Ctenidium

Mouth

05mm

FIG. 16. The Parilimyidae. Parilimya fragilis. A
ventral view of the mouth, lips and labial palps (re-
drawn after Morton, in prep.).

of lines, and at different times from this group
(Fig 17):

Runnegar (1974) especially has given an
excellent broad account of the fossil history of
the Anomalodesmata and their extinct repre-
sentatives. This paper concerns itself with the
extant anomalodesmatans with regard to
which much more detailed information is now
available.

All agree that the ligament is of prime taxo-
nomic importance in the Anomalodesmata
(Yonge, 1978; Runnegar, 1979; Yonge &
Morton, 1980) and it is this structure which
affords valuable clues as to the origins of the
various anomalodesmatan lineages.

Origin of the Thraciacea

The Thraciacea arose in the Mesozoic with
the Thraciidae constituting the oldest fossils.
Species of Thracia possess an external, pri-
mary ligament but with a characteristic, ante-
riorly located, lithodesma attached by resili-
fers direct to the valves. A relatively simple
body plan, long separate siphons, wide pedal
gape and an axe-like digging foot are features
that clearly previse the Periplomatidae and
Laternulidae.

In the Periplomatidae and Laternulidae,
however, the antero-dorsal region of the shell
arches over the postero-dorsal resulting in the
primary ligament swinging downwards to be
located between chondrophores. The over-
arching process is hinted at in the Thraciidae
and indeed so superficially similar are shells
of Thracia and Cochlodesma that Allen
(1961b) has mistaken them.

The superfamily remains infaunal but occu-
pies extremely specialized niches, most being
deep “passive” burrowers relying upon si-
phon withdrawal only (except Thracia) for de-
fense (Morton, 1973; 1981).

Origin of the Poromyacea (Poromyidae, Verti-
cordiidae and Cuspidariidae) (Newell, 1965,
1969) (the septibranchs)

The Anomalodesmata possess among the
most interesting of all bivalves, namely the
scavenging and carnivorous septibranchs.
The septibranchs comprise three generally
regarded discrete families—the Verticor-
diidae, Cuspidariidae and Poromyidae. High-
er taxonomic categories are, however, dis-
puted. Thus, Ridewood (1903) placed all
three families in the Poromyacea. Others, as
described earlier, link the Mesozoic Cuspi-

50 MORTON

CAENOZOIC

wae

`` MEGADESMIDAE
PERIPLOMATIDAE

CHAENOMYIDAE

THRACIIDAE

THRACIACEA

BURMESIIDAE

LATERNULIDAE

PHOLADOMYIDAE Maa
CLAVAGELLIDAE

CLAVAGELLACEA

PALAE OZOIC E>

PHOLADOMYACEA

MESOZOIC

EDMONDIIDAE MARGARITARIIDAE
\
N er,

MYOCHAMIDAE
PANDORIDAE

PANDORACEA

LYONSIIDAE

VERTICORDIIDAE

e 9°

PARILIMYIDAE
POROMYIDAE

POROMYACEA

( of Newell.1969)

FIG. 17. The adaptive radiation in the Anomalodesmata.

dariidae and Poromyidae in the Poromyacea
while the Caenozoic Verticordiidae are placed
in the Verticordiacea. Runnegar (1974)
placed the Verticordiidae in the Pandoracea,
the Cuspidariidae in the subclass Palaeo-
taxodonta (a now wholly discredited notion
(Yonge & Morton, 1980) originally formulated
by Purchon (1956b)) leaving only the Poro-
myidae in the Poromyacea. Bernard (1974)
concluded that the septibranchs were a
diphyletic terminal order within the subclass
Anomalodesmata dividing the families into
two superfamilies the Verticordiacea and the
Poromyacea (the Poromyidae and Cuspi-
dariidae). Subsequently, however, Bernard
(1979) has altered his views somewhat and
now considers all three families to have
superfamily status (the Verticordiacea be-
longing to the order Pholadomyoida and the
Poromyacea and Cuspidariacea belonging to
the order Septibranchoidea). Almost con-
versely, Allen and Morgan (in press) place the
Verticordiidae and Poromyidae in the Poro-
myacea and the Cuspidariidae in its own
superfamily. Morton (in prep.) elevates all
three families to superfamily status, deriving
all from a pholadomyacean ancestor possibly
similar to Parilimya and thus abandons the
order Septibranchoidea.

A recent study of Pholadomya candida
(Pholadomyacea) (Morton, 1980a) showed

that this species possessed a number of char-
acters possibly also possessed by some
“septibranchs.” Thus the sense organ
(opisthopodium) on the posterior region of the
visceral mass of Pholadomya is also appar-
ently possessed by Halicardia flexuosa (Dall,
1895), H. nipponense (Nakazima, 1967) and
Poromya eximia (Pelseneer, 1911). Possibly
significantly, Euciroa pacifica possesses
fused lips laterally and a medial lappet on the
posterior lip (Dall, 1895) also as in Pholado-
mya candida.

An examination of Parilimya fragilis (Mor-
ton, in prep.) has revealed even more striking
similarities between this pholadomyacean
and some of the septibranchs, notably mem-
bers of the less specialized Verticordiidae, but
also the much more specialized Cuspidariidae
and Poromyidae.

In particular, P. fragilis and members of the
Verticordiidae, e.g. Lyonsiella fragilis (Allen &
Turner, 1974), possess taenioid muscles
which are elongate components of the si-
phonal rectractors having separate insertions
on each valve. These, in both, may aid rapid
siphon withdrawal. Morton (in prep.) also sug-
gests that the posterior longitudinal septal
muscles of Cuspidaria can be derived from
the taenioid muscles of Parilimya. Similarly
the labial palps of P. fragilis have reduced
ridges and the lips are thickened, the anterior

THE ANOMALODESMATA 51

arching over the posterior as in many mem-
bers of the Poromyidae and Verticordiidae.
The lips of Lyonsiella formosa are fused
(Allen & Turner, 1974) like those of Phola-
domya candida (Morton, 1980a). Possibly
equally significant, however, is that the in-
halant siphon of Parilimya fragilis has the
same raptorial nature as that of members of
the Cuspidariidae and though lacking the
complex, apical sensory nerve endings of
Cuspidaria cuspidata (Reid & Reid, 1974)
and Cardiomya planetica (Reid & Crosby,
1980) the fundamental structure of the si-
phonal apparatus is the same. Most signifi-
cantly the intestine and stomach of Р. fragilis
are adapted for dealing with large pieces of
food, as in all “septibranchs.” There is thus
some evidence in Parilimya to indicate that a
verticordiid-cuspidariid line of evolution has
arisen from a pholadomyacean stock, and
not, аз suggested by Allen & Turner (1974)
and Runnegar (1974), from a pandoracean
(lyonsiid) ancestor.

Species of Parilimya may also have more to
reveal with regard to the origin of the Poro-
myidae. Very significantly, the ligament of P.
fragilis, indeed of all pholadomyaceans, is ex-
ternal as in members of the Poromyidae and it
seems at least possible that from a wider,
possibly as yet unstudied group of pholado-
myacean ancestors has arisen either two or
three major deep water, scavenging ano-
malodesmatan lineages, the most advanced
members of which have convergently evolved
to be highly specialized carnivores. Such an
interpretation finds general agreement with
that of Bernard (1974). At one time or other,
however (see Morton in prep. for a review),
the three constituent families of the Poro-
myacea (as defined by Newell, 1965, 1969)
have been variously linked one with the other
by numerous authors. Pending publication of
the review of the Cuspidariidae and Poro-
myidae by Allen & Morgan (in press), | prefer
to regard each family as a superfamily, but all
having a pholadomyacean ancestry. It seems
at least possible that each superfamily will
eventually be shown to comprise a number of
families: Bernard (1979) has already for ex-
ample divided the Verticordiacea into the
Verticordiidae and Lyonsiellidae.

The origin of the septum in the Poromyidae,
Cuspidariidae and some members of the
Verticordiidae is problematic. Dall (1890) con-
sidered the septum to be formed from the for-
ward extension of the siphonal retractor mus-
cles and the intersiphonal septum. This view

was supported by Plate (1897). Other authors
(Pelseneer, 1888a, b, 1891, 1911; Grobben,
1892; Ridewood, 1903; Yonge, 1928) con-
sider it to be derived from the ctenidia by a
reduction in the number of branchial aper-
tures and an increase in the degree of muscu-
larization. Bernard (1974, 1979) has reassert-
ed that the septum has a pallial origin. The
Origin of the septum seems to have been re-
solved by Allen & Morgan (in press) who have
recognised progressive degrees of gill reduc-
tion and septal development from the Verti-
cordiidae to the Poromyidae via the Cuspi-
dariidae. In Poromya and Cetoconcha, how-
ever, the anterior pedal retractor muscles
pass into the septum anteriorly to form the
inner longitudinal septal muscle. Similarly,
Allen & Morgan (in press) note that the outer
longitudinal septal muscle may have a pallial
origin. | find it very difficult to understand how
the pedal retractor muscles can become in-
volved in the muscularization of a septum in
which, undoubtedly, the major component is
ctenidial with pallial involvement. However,
Pholadomya candida is characterized by a
pair of pedal gape muscles that cross from
valve to valve, in front of the pedal gape and
serve as a mechanical “valve” with the foot
being used as a piston (Morton, 1980a). In-
corporation of these muscles into the septum
would seem a much more plausible sugges-
tion particularly with regard to the anterior
longitudinal septal muscles. Similarly the
taenioid muscles of Parilimya (Morton, in
prep.) (and Lyonsiella fragilis) (Allen &
Turner, 1974) would seem to be a logical pro-
genitor of the posterior longitudinal septal
muscles as originally postulated by Dall
(1890). In Pholadomya there can be seen the
first signs of the muscularization of the poste-
rior end of the ctenidium, and which is ulti-
mately fulfilled in the Cuspidariidae and
Poromyidae.

Clearly both Pholadomya candida and
Parilimya fragilis are highly specialized bi-
valves but collectively they have many fea-
tures reminiscent of the more modern Poro-
myidae, Cuspidariidae and Verticordiidae. A
more detailed investigation of other extant but
nevertheless rare pholadomyaceans may
provide more clues with regard to the origin of
the septibranchs.

In the Cuspidariidae rapid eversion and
withdrawal of the siphon is largely by the
translocation of blood from pallial lacunae to
the siphon and back. A similar mechanism is
required for Pholadomya candida extending

De MORTON

and retracting the foot so that the pallial
haemocoel is also large. It would seem that
the origin of the Cuspidariidae at least among
the septibranchs and the Clavagellacea can
best be explained by the exploitation of a
primitive means of rapidly changing fluids in
the mantle cavity, the former via the siphons
(and similar adaptations do also occur in
Parilimya), the latter via the pedal gape (as in
Pholadomya).

Origin of the Clavagellacea

The Clavagellacea have no known ances-
tors of more typically “bivalve” plan and the
Origin of this group has never been adequately
explained. The most important feature of the
infaunal clavagellids is that there is, as
described by Purchon (1956a, 1960) for
Brechites, a change of fluids between the
mantle cavity and the subterranean muds
mediated via the pedal gape. Extensive mus-
cles surround the pedal gape and form a
septum, which, by its movement up and down
forces water out of and into the infra-branchial
chamber through a wide, perforated plate—
“the watering pot’—of the adventitious shell.
The exact function of this action is unknown,
though it would hardly seem likely, as pro-
posed by Purchon (1960), that it functions as
a means of burrowing, except perhaps inci-
dentally, since the animal cannot be mobile—
the foot being imprisoned within the sealed
adventitious shell. Possibly the watering pot
acts as a Coarse sieve retaining material that
might enter the mantle cavity during pumping
of the septum. Fine particles penetrating the
sieve might constitute a source of food. In the
extinct Hippuritidae it seems that water was
drawn through the pores on the outer surface
of the left valve to be eventually trapped on
the broad and radially crenulate right mantle
margin (Skelton, 1976).

If this attributed function is correct then
Brechites can be compared with Pholadomya
candida which is also postulated (Morton,
1980a) to feed on deep deposits, via the
pedal gape. In this, albeit highly specialized,
member of the primitive Pholadomyacea a
pair of muscles arise from outside the anterior
adductor muscle and cross over anterior to
the pedal gape and attach to the opposite
valve at the pallial line. Contraction of these
muscles will close the pedal gape around, it
has been suggested, the foot which by re-
peated rapid expansion and contraction acts
as a suctorial piston with the pedal gape form-

ing a (mechanical) “valve.” Although the
Clavagellacea are clearly highly specialized,
modern bivalves with an adventitious shell,
they do share with Pholadomya candida the
distinction of being the only (known) anomalo-
desmatans in which the movement of fluids
via the pedal gape (for whatever reason) has
been hypothesized. Pedal feeding is not
unique to these bivalves. The Indo-Pacific
mangrove bivalve Polymesoda (Geloina)
erosa has been shown to feed this way, using
less sophisticated methods (Morton, 1976b).

Also significantly, clavagellids, like the
pholadomyaceans, possess an external liga-
ment and as in Pholadomya candida the
rectum passes beneath the heart.

It is thus suggested that the origin of the
infaunal Clavagellacea, i.e. Brechites, should
be sought amongst the Pholadomyacea and
that Pholadomya candida gives some insight
into how this superfamily arose. Clearly the
cemented members of the Clavagellacea
(Soliman, 1971; Smith, 1971), represented by
Clavagella, are a specialization from this
primitive infaunal stock with an appropriate
decrease in the pedal gape and greater reli-
ance upon the siphons for the exchange of
mantle fluids and the collection of potential
food. The genus Clavagella is, according to
Keen & Smith (1969), older than Brechites,
the former arising in the Upper Cretaceous,
the latter in the Upper Oligocene. However,
the thin shells of the latter may not fossilize
easily.

The cemented habit has arisen independ-
ently in other anomalodesmatan families,
notably the Cleidothaeridae and Myochami-
dae (Morton, 1974, 1977) and in the case of
the latter (Myochama) it is also assumed that
this has been from an infaunal ancestor
(Myadora) (Yonge & Morton, 1980). In all
cases, the evolution of the cemented habit in
the Anomalodesmata is a relatively recent
(Caenozoic) phenomenon.

Origin of the Pandoracea

The Pandoracea (as here redefined) arose
in the Caenozoic and though none possess
an external ligament, species of Lyonsia
possess an opisthodetic ligament, with a
ventral lithodesma, that Yonge & Morton
(1980) regard as primitive (to the Pandora-
cea).

In these bivalves there is a strong trend
towards valve inequality and the colonisation
of hard intertidal surfaces by means of byssal

THE ANOMALODESMATA 53

attachment in the Lyonsiidae and cementa-
tion in the Myochamidae and Cleidothaeridae.

Clearly, in the Pandoracea, there has been
adaptive radiation from a wide, relatively
modern stock to colonize widely diverse and
extremely narrow niches in coastal and in-
shore waters almost globally.

DISCUSSION

The extant Anomalodesmata are unusual
bivalves. They are diverse in both form and
habitat but a critical examination of them re-
veals first, basic, common underlying mor-
phological characteristics and second that
they occupy narrow, marginal niches. No-
where, except possibly in the deep sea, the
fauna of which is relatively sparse anyway
(compared with the littoral zone), are they
numerous. Each species is difficult to find.
Clearly they are a group the representatives
of which are highly specialized for life in highly
specific niches. Thus the lyonsiid Guiana-
desma sinuosum (Morrison, 1943) is only
known from the Essequibo drainage of British
Guiana; species of Cleidothaerus are only
known from Australia and New Zealand
(Morton, 1974); Offadesma angasi is similarly
only recorded from these waters (Morton,
1981), though Rosewater (1968) has shown
that the family Periplomatidae has an almost
global distribution, whereas the Laternulidae
is Indo-Pacific (Morton, 1976a).

There are relatively few extant anomalo-
desmatans each family often comprising but a
few genera and each genus only a few spe-
cies. There are, for example, probably only six
species of the single genus Laternula
(Laternulidae) (Morton, 1976a), but two
species (probably one) of Cleidothaerus (the
sole genus of the Cleidothaeridae) (Morton,
1974), and only some 30 species of the
Periplomatidae comprising the genera
Periploma and Cochlodesma (Rosewater,
1968) and one species of the Pholadomyidae
(Morton, 1980a). Because of their extremely
specialized habitats some probably await dis-
covery but nevertheless they are by any
standards rare. Pholadomya candida is
probably one of the rarest molluscs, only two
specimens ever having been found alive and
then from surf beaches after storms (Morton,
1980a). For many species, the habitats are
unknown.

Far, however, from being the remnants of a
primitive stock, in many cases, e.g. the

POROMYACEA (of Newell 1969 )

(+Porilimya branch of
PHOLADOMYACEA) colonise
deep water soft deposits

CAENOZOIC

4 > VENEROIDA

Generalist colonisers of inshore
soft deposits successfully
restrict Anomalodesmata to
more specialized niches

A>
7 PIERIOIDA

Colonise endo-and epibyssote
niches contining Pholadomyacea

to soft deposits AS

PHOLADOMYACEAN
stock

THRACIACEA
versify into specialized
infaunal niches

MESOZOIC di

PALAEOZOIC

FIG. 18. The origin of the various extant superfami-
lies of the Anomalodesmata.

Clavagellacea, Poromyacea and Pandora-
cea, they are relatively modern bivalves.
Some constant features of their anatomy,
however, Clearly link these modern bivalves to
the ancient, stem superfamiy Pholado-
myacea, with its origins in the Palaeozoic.
Thus, living representatives of the Anomalo-
desmata are like solitary pieces of a jigsaw
which though having a character of their own,
individually tell us little of their common an-
cestry. It is only when the jigsaw is con-
structed that a fuller picture can be obtained.
Unfortunately, however, the great majority of
the pieces are missing, because the Ano-
malodesmata have undergone phases of ex-
pansion and then massive retreat that makes
the construction of a lineage or an adaptive
strategy very difficult. An alternative analogy
is with a tree, the outermost twigs represent-
ing extant species of anomalodesmatans.
Many branches are missing, the pholado-
myacean trunk is represented by only a few
extent species and the root system is virtually
absent. What is attempted here therefore, is,
it is admitted, speculative.

The Pholadomyacea arose in the early
Palaeozoic (Fig. 18) and radiated into soft
sediments, becoming numerous and with the
Trigoniacea constituting the dominant com-
ponent of the late Paleozoic bivalve infauna
(Stanley, 1972; Yonge & Morton, 1980). Such
an assemblage, with these two groups domi-
nant, survived until at least the Cretaceous
(Hatai, Kotaka & Noda, 1969). At the same
time, the Pterioida were coming to dominate
the epifaunal niche, the neotenous retention

54 MORTON

and subsequent wide use of a byssal appa-
ratus by most representatives of this order
having far reaching consequences. Even
today, this ancient group has not been dis-
placed from its dominant position on hard,
marine surfaces. From the period of the late
Palaeozoic, we can obtain links in an
anomalodesmatan lineage that will take us to
the present day, notably with regard to a fairly
united group of families, the Thraciidae,
Laternulidae and Periplomatidae that Yonge
& Morton (1980) and Morton (19806) have
suggested (and which is now here formally
proposed) should constitute a separate
superfamily—the Thraciacea Stoliczka, 1870.

In many respects the extant species of
Thracia are a link with a pholadomyacean
stock, the external opisthodetic ligament
being a primitive feature (Runnegar, 1974;
Yonge & Morton, 1980). Also in Thracia we
see the first signs of an arching of the antero-
dorsal region of the shell over the postero-
dorsal, though a transverse umbonal slit is not
here developed. With a simple body plan,
large separate siphons, large ctenidia, simple
labial palps and a digging foot Thracia ade-
quately previses the more specialized Peri-
plomatidae and Laternulidae. In this line of
evolution should also be included the extinct
Burmesiidae (Morton, 1980a).

For most of the Anomalodesmata, how-
ever, the advent of the Mesozoic was a period
of declining importance (though they are
numerous in Jurassic and Cretaceous rocks),
probably because of competition with the now
expanding, generalist, order Veneroida.
These relatively unspecialized bivalves came
in the Mesozoic to dominate shallow water,
soft substrates—and still do. Effectively the
Pterioida and Veneroida have partitioned the
shallow water domain. From the Cretaceous
of India, Chiplonkar & Tapaswi (1976, 1977)
have described fossil communities of vener-
oids, pterioids and pholadomyoids. Thus by
the late Mesozoic, the Anomalodesmata were
surviving in narrow, restricted habitats, but
had also radiated into the deeper waters of
the sea where during this period a lineage or
more probably a number of lineages of bi-
valves arose all adapted to feeding either on
the rain of invertebrate carcasses falling from
the surface waters above or, ultimately, upon
living invertebrates, typically crustaceans that
were captured with a raptorial inhalant siphon.
These bivalves constitute the Poromyacea, in
the widest definition of the term, but here now
divided into the Poromyacea (Poromyidae),
Verticordiacea (Verticordiidae) and Cuspi-

dariacea (Cuspidariidae). In this environ-
ment these bivalves have become relatively
numerous. Knudsen (1979) has shown that in
bathyal and abyssal depths, the Anomalo-
desmata, together with another ancient
group, the Palaeotaxodonta, similarly largely
excluded from the littoral zone and fringe,
have become dominant. In inshore waters,
however, the other members of the Ano-
malodesmata, excluding the septibranch
superfamilies, occur as scattered descend-
ants of a once populous group.

In the Caenozoic, however, the Ano-
malodesmata, represented mainly by the
Clavagellacea and the Pandoracea have
undergone a further, narrower, phase of ex-
pansion. In this period they have diversified
from their ancestral mode of life and produced
families which are for example byssally at-
tached (e.g. the Lyonsiidae) and even families
which are cemented, e.g. the Clavagellidae,
Cleidothaeridae and Myochamidae. Conveni-
ently some representatives of the Clavagelli-
dae and the Myochamidae are uncemented,
infaunal species, that permit comparison with
their cemented colleagues, allowing us to
understand more easily this phase of adaptive
radiation. In highly specialized niches these
bivalves too enjoy a measure of success.

The Anomalodesmata are characterized by
a number of very important features. Possibly
the most significant of these is concerned with
reproduction. With the possible exception of
the Cuspidariidae, which are dioecious
(Bernard, 1979), all anomalodesmatans are
simultaneous hermaphrodites. It has also
been shown for the Pandoridae (Allen,
1961a), Periplomatidae (Morton, 1980b), and
for Pholadomya candida and the deep water
members of the Poromyacea (Morton, 1980a;
Knudsen, 1979) that large, telolecithal eggs
are produced which are often encapsulated.
The precise reason for this is unknown but
can be interpreted in two ways (Morton,
1980a). Possibly the large amounts of yolk
provide nourishment for the developing em-
bryo over a long period of time while it is also
protected and possibly made buoyant by the
capsule. Spermatozoa may be embedded in
the capsule, to fertilize the egg later, possibly
after a period of dormancy in the plankton.
These would be adaptations for a long pelagic
larval stage. Alternatively, fertilization may oc-
cur within the common urinogenital cloaca
typical of many of these bivalves or the supra-
branchial chamber and development of a
large larva, requiring large amounts of yolk
may be rapid but also taking place within the

THE ANOMALODESMATA 55

protective confines of the capsule. Allen
(1961a) has shown that development is ex-
tremely rapid in Pandora inaequivalvis and is
completed within four days, the veliger spend-
ing less than one day in the plankton. Allen
considers this an adaptation to /imiting the
spread of juveniles so that the species rapidly
recolonizes the parental habitat before the
larvae can be washed away. This of course is
opposite to the vast majority of the Pterioida
and Veneroida where oligolecithal eggs are
released for colonization of new habitats
further afield. A notable exception to this role
in the Veneroida are members of the
Leptonacea which produce large eggs—but
they too occupy extremely specialized niches
and as with the Anomalodesmata are
monoecious, though typically protandrous
consecutive hermaphrodites (Morton, 1980b).
Large eggs are also characteristic of bathyal
bivalves (Knudsen, 1979) and most ano-
malodesmatans from this habitat have either
a very short, non-feeding larval stage or no
pelagic stage at all. Thus, hermaphroditism
and rapid development, in all species, is an
essential requisite for their successful occu-
pation of their narrow niches. To the contrary,
however, such characteristics are completely
the opposite of those possessed by the gen-
eralist Pterioida and Veneroida and it is easy
to see how the Anomalodesmata have con-
sistently failed in competition for broader
habitats.

The shell of anomalodesmatans is relative-
ly uniform, generally comprising a prismato-
nacreous aragonite or being of a homogene-
ous nature (Taylor, Kennedy & Hall, 1973).
Only with regard to the ligament, however, are
there significant differences between the
superfamilies.

The primitive condition is represented by
the Pholadomyacea, with an external primary
ligament. This is retained in Thracia
(Thraciacea), with the addition of an anterior
lithodesma, and members of the Clavagella-
cea and Poromyacea of the more modern
lineages and provides compelling evidence of
the manner in which the Anomalodesmata
have diversified from a pholadomyoid stock.
Thus, the presence of an external ligament in
the Clavagellacea lends support to the notion
that this group arose from a pholadomyid
stock which have evolved (like P. candida)
pedal feeding. Similarly it is possible to sug-
gest a link between the pholadomyacean
Parilimya and the Poromyacea because of
similar features and the common presence of
an external ligament. Finally, Thracia may

well be a link between the Pholadomyacea
and the more specialized Periplomatidae and
Laternulidae and, again, the presence of an
external ligament supports this. In the other
superfamilies the ligament sinks to become
internal (a possibly intermediate condition is
seen in the Ceratomyacea with a bilaterally
asymmetrical ligament (Runnegar, 1974)).
Thus in the Lyonsiidae, probably representing
a more primitive condition (Yonge & Morton,
1980), the ligament is opisthodetic, with the
development ventrally of a lithodesma, by
calcification of a central strip of the inner liga-
ment layer. The lithodesma serves to make
an otherwise inefficient ligament more effec-
tive as explained by Yonge & Morton (1980).
Variations on this theme characterize the re-
mainder of the Pandoracea, Verticordiacea
and the Cuspidariacea—the most modern
anomalodesmatan lineages.

In the Thraciacea the ligament is located in
a dorso-ventral plane and the lithodesma,
where present, is anterior and the antero-
dorsal edge of the shell arches over the pos-
tero-dorsal. The transverse crack in the shell,
characteristic of the Periplomatidae and Later-
nulidae, but not obvious in the Thraciidae,
facilitates an unusual method of valve adduc-
tion, at least in the Laternulidae (Morton,
1976a), to effect an exchange of water be-
tween the mantle cavity and the sea.

A lithodesma is not present in all repre-
sentatives of families which characteristically
possess one, being absent in, for example,
Guianadesma in the Lyonsiidae (Morrison,
1943), in Offadesma in the Periplomatidae
(Morton, 1981) and in different species of the
single genus Laternula comprising the
Laternulidae (Morton, 1976a). It is thus not a
prerequisite for any functional mode of opera-
tion of the shell but probably rather improves
upon an established design. A lithodesma is
also not absolutely characteristic of the
Anomalodesmata; one is found in Montacu-
юпа compacta (Leptonacea) (Morton,
1980b). Nevertheless a ligamental lithodesma
is a recurring, though inconsistent, feature of
the living Anomalodesmata.

In most species, mantle fusion is of folds
additional to the inner, so that the margins
and the siphons tend to be thick and often
covered in periostracum. Radial mantle
glands are found in representatives of the
Lyonsiidae (Prezant, 1979), Verticordiidae
(Allen & Turner, 1974), Periplomatidae
Morton, 1981) and in Parilimya fragilis (Mor-
ton, in prep.). They produce a glue which
sticks sand grains to the periostracum though

56 МОАТОМ

the significance of this is not understood.
Often the mantle margin possesses a fourth
pallial aperture. Such an aperture also occurs
in members of the Solenidae and Mactridae
where it acts as a pressure release “valve” in
these fast burrowing bivalves (Yonge, 1948).
In Pholadomya candida a similar function
was envisaged but here as a mechanical
“valve” to prevent damage either to the thin
shell or to the various organ systems of the
body (Morton, 1980a) during pedal feeding,
when powerful pressures are built up in the
mantle cavity. Where it occurs in other
anomalodesmatans, e.g. the Thraciidae
(Allen, 1954), Lyonsiidae (Yonge, 1952;
Narchi, 1968), Myochamidae and Cleido-
thaeridae (Morton, 1974, 1977), its function,
because of so contrasting life styles, is less
obvious. In yet other anomalodesmatans, e.g.
the Pandoridae, Periplomatidae (Allen, 1954,
1958) and Laternulidae (Morton, 1973) it is
absent.

With the exception of the Cuspidariidae and
Poromyidae, gill structure and ciliation in the
Anomalodesmata are remarkably constant.
The ctenidia comprise a complete inner and a
reduced outer demibranch composed of the
descending lamella only. The labial palps and
lips of the mouth are typically of the normal
bivalve type though in the Pholadomyacea
and the Poromyacea and Verticordiacea they
are modified. In Pholadomya candida, the
lips form two fused lateral pouches which pre-
vent food being flushed out of them whereas
in the latter two superfamilies and in Parilimya
(Pholadomyacea) they are reduced, muscu-
larized and have fewer sorting grooves—all
adaptations to a macrophagous feeding style
(Allen & Turner, 1974).

Another, unusually variable feature is the
degree of association between the heart and
the rectum. The rectum may pass beneath it,
e.g. Pholadomya (Morton, 1980a), penetrate

Pholadomyacea Gray, 1847
Thraciacea Stoliczka, 1870

Clavagellacea d’Orbigny, 1844
Pandoracea Rafinesque, 1815

Poromyacea Dall, 1886
Verticordiacea Stoliczka, 1871
Cuspidariacea Dall, 1886

it as in members of the Periplomatidae and
Laternulidae (Allen, 1958; Morton, 1973) or
pass above it, e.g. Cleidothaerus (Morton,
1974).

The stomach and the style sac seem uni-
form in structure and of Type IV (Purchon,
1958) except т Cuspidaria, Poromya
(Purchon, 1956b) and Parilimya (Morton, in
prep.) where there is a simplification of form
associated with a macrophagous life style and
the development of an extensive chitinous
lining and a reduction in sorting areas. This is
the stomach type Il of Purchon (1956b).
Bernard (1974) has investigated, in detail,
features of the stomach of members of the
Verticordiidae, Cuspidariidae and Poro-
myidae and shown them to be clearly differ-
entiated into two groups. The Poromyidae
and Cuspidariidae are very similar, possibly
because of very similar feeding styles,
whereas that of the Verticordiidae is much
more like that of other eulamellibranchs with a
small gastric shield and a well-developed food
sorting caecum. Almost certainly Parilimya
(Pholadomyacea) is a link in the evolution of
the carnivorous habit in the Cuspidariidae,
Poromyidae and some members of the
Verticordiidae (Morton, in prep.)

The apparently random assignment of
many of these characters to the various repre-
sentatives of the Anomalodesmata makes it a
difficult group to understand and clearly the
picture of them and their ancestry is only
going to clarify when each is studied individ-
ually.

SUMMARY

The subclass Anomalodesmata Dall, 1889
is judged to comprise one order Pholado-
myoida Newell, 1965, seven extant super-
families and 13 families as follows:

Pholadomyidae Gray, 1847
Parilimyidae Morton, 1981
Thraciidae Stoliczka, 1870
Periplomatidae Dall, 1895
Laternulidae Hedley, 1918
Clavagellidae d'Orbigny, 1843
Lyonsiidae Fischer, 1887
Pandoridae Rafinesque, 1815
Myochamidae Bronn, 1862
Cleidothaeridae Hedley, 1918
Poromyidae Dall, 1886
Verticordiidae Stoliczka, 1871
Cuspidariidae Dall, 1886

THE ANOMALODESMATA 57

The stem superfamily Pholadomyacea
arose in the Palaeozoic and was largely con-
fined to soft inshore sediments because the
endo- and epibyssate modes of life were prin-
cipally occupied by the Pterioida. In this
habitat they widely radiated producing a
large number of taxa (Runnegar, 1974).
One of these adaptive assemblages—the
Thraciacea—still survive with the Thraciidae
as the link with the Pholadomyacea. In the
Mesozoic, however, the Pholadomyacea ap-
pear to have been largely displaced by the
evolving heterodont Veneroida, but they were
ideally preadapted to survive in deep water,
where they are now a major component com-
posed of up to three lineages, the Verticor-
diacea, Cuspidariacea and Poromyacea, all
of which have evolved from the Pholado-
myacea possibly independently but from
similar stocks that may find common origin in
the pholadomyacean Parilimya and its an-
cestors. Comparatively recently, in the
Caenozoic, two further superfamilies have
evolved—the Clavagellacea and Pan-
doracea—which have widely radiated into
various shallow water niches, both groups
producing cemented genera and the latter
byssally attached genera for exploitation of
specialized hard niches.

In general terms the representatives of the
Anomalodesmata are characterized by a
number of features, but probably the most
significant of these is the occurrence in all
(except the Cuspidariidae) of simultaneous
hermaphroditism and a short, pelagic larval
life. These are adaptations to colonization of
narrow niches and adequately explain how
the group has been unable to survive com-
petition with the more generalist Pterioida and
Veneroida which are typically dioecious pro-
ducing large numbers of oligolecithal eggs
and long-lived larvae that may be widely dis-
persed.

The evolution of the Thraciacea and Pan-
doracea from a primitive pholadomyacean is
fairly easily understood especially in the
former superfamily where the Thraciidae form
a Clear link.

In the case of the hitherto unexplained
Clavagellacea, however, a study of the rare
pholadomyacean Pholadomya candida has
indicated that Brechites can be derived from a
pholadomyacean ancestor in which occurs an
exchange of mantle fluids via the pedal gape.
In the case of Pholadomya this is thought to
be a feeding current; possibly this is also true
of the Clavagellidae, but is uncertain.

Similarly, the evolution of the Poromyacea,
Cuspidariacea and Verticordiacea can pro-
ceed from pholadomyacean ancestors similar
to the extant genus Parilimya, a study of one
species of which has shown it to possess all
the prerequisites essential for such a transi-
tion including features that will lead all
lineages, convergently, into the scavenging
and ultimately the carnivorous mode of life.

The Pholadomyacea were predisposed to
the rapid movement of water into and out of
the mantle cavity, by rapidly channelling blood
into the haemocoel between the mantle
epithelia. This is also seen in the Clavagellacea
and the Poromyacea, Cuspidariacea and
Verticordiacea; possibly enabling the unusual
feeding methods thought typical of these
groups.

The adaptive radiation in the Anomalo-
desmata must be seen as the evolution of a
group, once widely successful, but surviving
now in narrow, specialized niches and
demonstrating a wide diversity of adaptations,
reflecting a long and varied history, and the
extant superfamilies of which have arisen at
various times.

ACKNOWLEDGEMENTS

| am grateful to Sir Maurice Yonge (Univer-
sity of Edinburgh) and Dr. Bruce Runnegar
(University of New England, Armidale, Austra-
lia) for their critical reading of the first draft of
the manuscript of this paper.

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60 MORTON

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MALACOLOGIA, 1981, 21(1-2): 61-93

THE FUNCTIONAL MORPHOLOGY AND EVOLUTION OF RECENT
LIMOPSIDAE (BIVALVIA, ARCOIDEA)

P. Graham Oliver

Department of Zoology, National Museum of Wales, Cathays Park,
Cardiff СН 3NP, United Kingdom

ABSTRACT

The bivalve family Limopsidae is divided into thirteen morphological classes which have not
previously been recognized. These classes are defined from both shell and anatomical features.
Of the former the most relevant are the degree of anterior reduction, tumidity, periostracal
bristles, hinge and ligament, and of the latter the pedal, byssal and gill axis musculature. One of
the most significant morphological observations is the recognition of four ligament types within
the family. The morphological classes are sorted into three major functional groups—Limopsi-
form, Glycymeriform and Abyssate Burrowing.

The Limopsiform group contains eight of the morphological classes; in general these are
semi-infaunal with degrees of endobyssate and epibyssate attachments. There are three com-
ponents: 1. Ploughing. Mobile crawlers through soft substrates or over hard substrates rarely
employing a byssus. 2. Endobyssate. Less mobile, generally infaunal employing a multiple-
stranded byssus. 3. Epibyssate. Epifaunal with a well-adapted byssus of multiple strap-like
threads.

The Glycymeriform group contains two classes which show a marked convergence with the
Glycymerididae and are poor shallow burrowers: 1. A ribbed sculptured class with a wide Recent
distribution. 2. A finely decussate sculptured class with a restricted range in southeast Australia.

The Abyssate Burrowing group contains three classes which may not be closely related, yet
do have an antipodean bias in their distribution. Two classes are limited to southeast Australia
and contain small species with some affinities with the Glycymeriform group. These are argued
to be poor burrowers in sands and gravels. The third class is endemic to Antarctica and is
hypothesized to contain shallow burrowers living in muddy substrates.

The evolutionary history of the Limopsidae indicates an early Cretaceous semi-infaunal origin
with rapid radiation into the Limopsiform classes by the late Cretaceous. There was little func-
tional radiation within the Limopsiform group after the Cretaceous, but there must have been a
subsequent parallel morphological radiation giving rise to those species with the more advanced
ligament structure. An early offshoot of this semi-infaunal group was the Glycymeriform line
which appeared in the middle Cretaceous. The Glycymeriform and the Abyssate Burrowing
groups, excluding the Antarctic one, had a Mid-Cenozoic radiation in the antipodean provinces,
but declined in the northern hemisphere. The Antarctic class is apparently recent in origin and,
significantly, possess the most advanced ligament form.

The extent of the radiation is compared with that of other byssate and burrowing arcoids and,
although it is considered to be relatively wide functionally, it is not so morphologically, nor are the
species diversity and distribution comparable.

A preliminary analysis suggests that the growth and morphological features of the limopsid
ligament prevented radiation into the anteriorly reduced byssate forms in all except the most
minute species, and that the same ligament could also not be adapted to achieve enough
strength to allow radiation into the burrowing habit. The family as a whole, therefore, remained
semi-infaunal. However, semi-infaunal bivalves had already been largely excluded by advanced
burrowing heterodonts and consequently the limopsids were restricted to environments where
competition was less extreme, e.g. the deep sea.

INTRODUCTION Glycymerididae and Philobryidae, although
the exact nature of the relationship is not

The Limopsidae are a small family of arcoid agreed upon (Tevesz, 1977; Nicol, 1950).
bivalves which because of their generally The Limopsidae and Philobryidae are of
deep water distribution have received little at- considerable interest with regard to the adap-
tention. The affinities of the family are with the tive radiation of the Arcoidea. They represent

(61)

62 OLIVER

the only extant forms which lack the typical
chevron (duplivincular) ligament. They also
possess compressed, rounded or oval shells
which contrast markedly with the quadrate
shells of the Arcacea. Thomas (1976) outlined
the adaptive limitations of the duplivincular
ligament, but it is apparent that in terms of
species diversity, habitat range and geographi-
cal range the Limopsidae and Philobryidae
are even more restricted.

By examining both the functional morphol-
ogy and evolution of the oldest family, the
Limopsidae, this paper aims to develop an
hypothesis to explain at least in part why there
are such restrictions.

MATERIALS AND METHODS

Previous studies on limopsids have on the
whole not taken into account the variability of
shell form which arises through ontogeny or
ecological factors (Dell, 1964; Knudsen,
1967, 1970; Oliver & Allen, 1980b). This has
led to the erection of an unnecessary number
of species and genera. For this reason it is
not possible to discuss morphology or radia-
tion using current systematic groupings.
Ninety percent of the known Recent species
have been examined in this study. Of the fifty
species, eighteen were obtained with intact
soft parts. Observations based on them have
been used to construct a revised classifica-
tion. Due to nomenclatural problems, all spe-
cies have been placed in Limopsis sensu lato.
The diagnoses of these morphological
classes are presented in the Appendix which
provides notes on habitat, depth range, geo-
graphical range and species included in each
class. Throughout the text the morphological
classes are referred to numerically: M.C. | to
М.С. XIII. Note that the figures are in two ser-
ies: Figs. 1 to 12, and App.[endix] Figs. 1 to
27:

KEY TO ABBREVIATIONS OF INSTITU-
TIONS FROM WHICH FIGURED
SPECIMENS WERE OBTAINED

AMS Australian Museum, Sydney

BMNH British Museum (Natural History),
London

IRSNB Institut Royal des Sciences Natur-
elles de Belgique, Brussels

MCZ Museum of Comparative Zoology,

Harvard University

MNHNP Museum National d’Histoire Natur-

elle, Paris
NM Natal Museum, Pietermaritzburg
NMW National Museum of Wales, Cardiff
NSMT National Science Museum, Tokyo
RSM Royal Scottish Museum, Edinburgh
SAM South Australian Museum, Adelaide
USNM United States National Museum,

Washington, D.C.

FUNCTIONAL MORPHOLOGY

Studies on the morphology of limopsids are
very few. Pelseneer (1888) described the
morphology of Limopsis cancellata (Reeve,
1843) and Burne (1920) did likewise with L.
marionensis Smith (1885). Purchon (1957)
and Dinamani (1967) described the anatomy
of the stomach of L. vaginata Dall (1891) and
L. belcheri (Adams & Reeve, 1850) respec-
tively. Little functional interpretation, if any,
was made in these studies. Jeffreys (1864)
observed living L. aurita (Brocchi, 1814) and
noted its ability to crawl on a smooth surface
and to produce a byssus consisting of a single
fine thread. Atkins (1951) noted that the ciliary
currents are like those of Glycymeris glycy-
meris and Arca tetragona (Atkins, 1936).

Tevesz (1977) studied both the Philobryidae
and Limopsidae, basing his conclusions pri-
marily on observations made on two live
Australian species, Limopsis loringi Angas
(1873) and L. soboles (Iredale, 1931). Tevesz
concluded that in general limopsids are con-
vergent with the Glycymerididae, being poor
shallow burrowers with an endobyssate at-
tachment. Tevesz, however, also noted that L.
antillensis Dall (1881) is convergent with the
philobryid genus Cratis and that philobryids
are generally epibyssate.

Oliver (1978) and Oliver & Allen (1980b)
examined the functional morphology of the
deep water Atlantic species with special refer-
ence to adaptations for this habitat. They noted
a larger variety of habits than was suggested
by Tevesz’s study. Examination of live L. aurita
showed that this species typically ploughs
through the surface of soft sediments, remain-
ing in a vertical position in muds but falling onto
one valve in sands. It was also observed to
crawl over gravels and was able to suspend
itself by its byssus from larger stones or the
sides of the aquarium. The large abyssal spe-
cies Limopsis tenella Jeffreys (1876) (=
pelagica Smith, 1885) was also suspected to
be a ploughing form, but from the distribution

RECENT LIMOPSIDAE 63

FIG. 1. Reconstructions of life positions. A. Limopsis marionensis (М.С. |). В. L. vaginata (М.С. Ill).

FIG. 2. Reconstructions of life positions of species in M.C. V. A. Limopsis affinis. B. L. diegensis. C. L.

oblonga.

and size of some of the shell epifauna it was
further concluded that much of its life must be
spent lying on one valve. The byssus was rare-
ly observed in L. tenella. A much smaller spe-
cies, L. cristata Jeffreys (1876) (including L.
affinis Verrill, 1885), was shown to be more
infaunal, with a multiple, but finely threaded
byssus. L. minuta (Philippi, 1836) was sus-
pected to be, to a great extent, epibyssate.
The morphological variety exhibited in the
thirteen classes is greater than any suggested

by previous studies. This variety is, however,
expressed in relatively minor differences of
shell and anatomical detail. Functionally signif-
icant shell characters are the outline, tumidity,
anterior reduction, marginal crenulations and
hinge strength. Anatomical characters of im-
portance are the foot, byssus apparatus, gill
axis musculature and mantle margin muscula-
ture. Using these characters it is possible to
recognize three major groups containing
morphological classes with a high degree of

64 OLIVER

Deo: SL De
0.00.5 De > en

one?

FIG. 3. Reconstructions of life positions. A. Limopsis natalis (М.С. VIII). В. L. elachista (М.С. VIII). С. L

minuta (М.С. VII).

EPIBYSSATE

PLOUGHING

ENDOBYSSATE

FIG. 4. Tumidity and anterior reduction in relation to limopsid habits.

functional similarity: 1. Limopsiform. (М.С. |-
М.С. VII). Shell thin, strongly oblique, hinge
weak, heteromyarian condition advanced.
Foot with a long toe, byssus functional, gill axis
muscular. 2. Glycymeriform. (М.С. IX-M.C.
X). Shell thick, oblique, hinge strong, hetero-
myarian condition moderate. Foot blade-like,
byssus functional, gill axis weakly muscular. 3.
Abyssate. (М.С. XI-M.C. XIII). Subequilater-
al, almost elliptical, hinge moderate, almost
isomyarian. Foot blade-like, byssus not func-
tional in adult, gill axis feebly muscular.

Limopsiform group

Within the limopsiform classes there 15 а
series of linked progressive character changes
which indicate a range of life modes from
‘ploughing’ through endobyssate to epi-
byssate. This progression is linked to the
strength and use of the byssus, involving re-
lated changes in pedal morphology and shell
characters.

The ligaments found within the limopsiform
group are of Types A, B and C (App. Fig. 1).

RECENT LIMOPSIDAE 65

<:
<=

D
к,

FIGS. 5-8. Reconstructions of life positions. Fig. 5. Glycymeriform. A. Limopsis multistriata (M.C. IX). В. L.
bassi (М.С. IX). Fig. 6. Glycymeriform. A. L. loringi (М.С. X). B. L. eucosmus (М.С. IX). Fig. 7. Abyssate
Burrowing L.lilliei (М.С. XII). Fig. 8. Abyssate Burrowing L. vixornata (М.С. XI).

66 OLIVER

However, there is apparently no relation be-
tween the ligament type and habits. In liga-
ment Types A and B there are both ploughing
and epibyssate species and a similar range
occurs in species with the Type C ligament.
The detailed function of these ligaments re-
quires evaluation, but for the present, without
suitable material, little can be done.
Ploughing (M.C. I-M.C. IV): The behaviour
of Limopsis aurita (М.С. IV) т soft sediments is
typical of the ploughing mode (App. Fig. 12).
Effectively, the behaviour is crawling, with
depth of penetration depending on the resist-
ance of the substrate. The long toe is capable
of considerable extension and the animal is
progressively pulled across or into the sub-
strate, there being no stationary burrowing
motions. The long sole created by the exten-
sion of the foot into the toe and heel gives a
stable crawling base. Conversely, this foot
form is not adapted for efficient burrowing. The
heteromyarian condition, weak hinge and
weak ligament, are also indicative of a non-
burrowing habit. The compressed shell acts as

a blade and aids substrate penetration, but if
this is not achieved the animal is unstable in an
upright position. The byssus, although weak, is
frequently employed in L. aurita and gives
some anchoring effect. The byssus activity is
reflected in the presence of a small byssus

Imm

FIG. 9. Limopsis minima Sow. (= oolithica Buvig-
nier) with ligament area enlarged to show remains
of obliquely grooved ligament.

FIG. 10. Some early Cretaceous limopsids. A. Limopsis albiensis Woods. B. L. coemansi Briart & Cornet. C.
L. hoeninghausii Müller.

RECENT LIMOPSIDAE 67

FIGS.
Adams). Capped prodissoconch (Fig. 11) and
marginal locking groove (Fig. 12).

11-12. Nipponolimopsis decussata (A.

retractor element in the posterior pedal re-
tractor (App. Fig. 11). A consequence of this
variability in substrate penetration is the incon-
sistent positioning and size of the inhalant
aperture. Oliver & Allen (1980b) observed that
frequently the whole limit of the shell gape was
open. This led to considerable amounts of un-
wanted matter entering the mantle cavity and
this was frequently expelled by gill contraction
and valve clapping. This behaviour explains
the large amounts of axis muscle in L. aurita
(App. Fig. 11). In soft sediments the gape was
reduced and the mantle cavity was protected
by interlocking edges of the periostracal
interlocking edges of the periostracal bristles.

This apparently generalised form provides a
good interpretive base. Limopsis marionensis
(App. Fig. 2 and 5; М.С. 1) is a considerably
larger species, is more compressed and the
anterior margin is more rounded. The two latter
features further aid substrate penetration and
Stabilisation respectively. The posterior pedal
retractor has no separate byssus element and

the rare occurrence of the byssus thread sug-
gests that the ploughing habit is employed and
is probably more efficient than in L. aurita
(M.C. IV). Observations on another species (L.
tenella) showed that the umbonal and poste-
rior portions were most heavily infested, again
adding to the premise that M.C. | species are
semi-infaunal (Oliver & Allen, 1980b). M.C. |
species are almost exclusively found in soft
sediments where endobyssate anchoring is
least necessary. L. marionensis has been re-
corded from coarser substrates and here this
species must be surface-living. In all sub-
strates it is expected that frequent dislodgment
will occur and that surface positions will not be
uncommon.

In all characteristics other than the inner ser-
rated margin and ligament, the species of M.C.
| (App. Fig. 3) are identical morphologically to
M.C. | and are also presumed to be ploughers.
The serrated margin is a weak form of marginal
crenulation which more commonly occurs in
the endobyssate and epibyssate species.

The presence of the cleft in Limopsis
vaginata and L. cumingi A. Adams (1862)
(App. Fig. 4; М.С. Ill) is no doubt of some func-
tional significance, but without direct obser-
vations it remains obscure. The ontogenetic
development of the cleft (App. Fig. 7) clearly
shows that it is analogous to the small inden-
tations seen at either end of the dorsal area in
many typical species. It is, therefore, tempting
to associate the cleft with the hinge mechan-
ics. In L. vaginata the hinge plate, because of
its restriction to a shorter area, is more arched
and probably stronger. The advantage of this
in an otherwise ploughing form is obscure.
Another consequence of the cleft is the spout-
ing or projecting of the postero-ventral mar-
gin. Fig. 1 shows L. vaginata and a typical
M.C. | form orientated along the same axis. In
L. vaginata the major inhalant area is raised
higher in the water column. This spouting ef-
fect may help to cut down the amount of sub-
strate derived matter entering the mantle cav-
ity.

Endobyssate forms (М.С. V-M.C. VI): A
more sedentary infaunal habit is evidenced in
some of the smaller limopsiform species by
the presence of a multiple, long, fine-stranded
byssus and a separate byssus element (App.
Fig. 13) in the posterior pedal retractor. The
byssus threads have no terminal disc and
have small sediment particles attached along
their length. This strong evidence of endo-
byssate attachment is substantiated by other
features. The periostracal bristles are gener-

68 OLIVER

ally spicate (App. Fig. 9) and act in a manner
similar to shell spines, i.e. as a stabilising
mechanism. This type of periostracum no
longer acts as a protective grid and the mantle
margins in some species are more muscular,
indicating their ability to form discrete inhalant
and exhalant apertures.

The outline and relative tumidity are some-
what variable and this gives a variety of orien-
tations to the endobyssate species (Fig. 2).
The majority are relatively compressed and
have a tendency towards a straight anterior
margin, e.g. Limopsis cristata and L. affinis.
In L. affinis this development reaches its ex-
treme, giving a pseudo-modioliform ap-
pearance. The orientation of this form is prob-
ably sub-surface with the greater part of the
shell not buried. Shell epifauna data from
Oliver & Allen (1980b) support this conjecture.

In the more rounded forms which in some,
e.g. L. oblonga A. Adams, 1860 (App. Fig. 14),
are relatively tumid, a deeper position is hy-
pothesized. The rounded, less oblique outline
is consistent with the burrowing species and
the true ploughing forms. In muds, which are
the most common habitat for these species,
penetration would not be difficult. In fact, the
tumidity may be a stabilising influence pre-
venting the animal from becoming buried
beyond the postero-ventral margin. L.
galathea Knudsen, 1970 (М.С. VI) represents
the extreme of this fixed infaunal habit (Oliver
& Allen 1980b), the reduced heteromyarian
condition, stubbly periostracum and relative
tumidity are indicators of this. L. galathea
lives in soft abyssal oozes where overpene-
tration is very likely.

The larger compressed species Limopsis
diegensis Dall, 1908 (App. Fig. 10) with its
thatched periostracum outwardly resembles a
ploughing form; anatomically it is endo-
byssate. This intermediate character probably
reflects a more active habit as a plougher.
Ploughing activity by the endobyssate forms
is probably common as all species possess a
long-soled foot. Physical and biological dis-
turbance is probaby a frequent occurrence
and the ability to crawl away and re-establish
itself would be advantageous.

In all the endobyssate forms the inner mar-
gin is evenly crenulated by raised ridges or
nodules. In these small species this character
is regarded as a counteracting mechanism to
the weak hinge and ligament. It is presumed
to prevent shearing of the valves which may
be caused by physical or biological dis-
turbance.

Epibyssate forms (М.С. VII-M.C. VIII; Fig.
3): The epibyssate mode is evidenced in the
limopsiform group through the strength of the
byssus and the classically associated shell
characteristics of tumidity and anterior reduc-
tion (Stanley, 1972) (Fig. 4). The byssus con-
sists of three to six short strap-like strands
attached to a basal sheath. They have divided
ends with no terminal discs, but have been
observed firmly attached to particles of gravel.
In М.С. VIII (App. Fig. 16), the outline of the
shell is quadrate with a marked antero-dorsal
straight margin. This straight edge gives a
stable area on which the shell can rest. The
tumidity of these forms is relatively great and
this prevents toppling. The quadrate outline of
М.С. VII (App. Fig. 15; Limopsis minuta) is
less and it is presumed that this group is not
so highly adapted to the epibyssate mode.

In both М.С. VII and М.С. VIII the anterior
reduction is advanced, but the anterior ad-
ductor and anterior hinge teeth are never lost.

The byssus retractor systems in the two
classes are different. The minute forms of
М.С. VIII have no separate byssus retractor
element. No specimens have been available
to carry out detailed anatomical studies; it is
presumed that the posterior pedal retractor is
large enough to assume this role. The condi-
tion may be even more extreme where the
posterior retractor has its main muscle attach-
ments to the byssus gland rather than to the
base of the foot. In the larger М.С. VII class a
highly specialized byssus retractor is present
(App. Fig. 17) and this may be a function of
the larger size, but may also be related to the
less adapted shell outline. The less quadrate
form of Limopsis minuta is less stable and
to counteract this, the byssus retractor is
stronger.

Marginal crenulations reach the peak of de-
velopment in the epibyssate forms and their
restriction to the postero-ventral margin is un-
doubtedly linked to the high degree of anterior
reduction. In these forms the hinge no longer
acts as a major valve-locking mechanism, this
being taken over by the posterior adductor. To
prevent shearing around the adductor, a new
pseudo-hinge is formed across the adductor
utilising the now small true hinge at one end
and the postero-ventral crenulations at the
other.

Intermediate forms may be represented by
Limopsis elachista Sturany (1899) which,
while possessing a ‘strap’ byssus, does not
become quadrate until late in its development.
This species may be partially endobyssate.

RECENT LIMOPSIDAE 69

Unfortunately, no observations on live ani-
mals are available for this group and although
Fig. ЗС shows the minute quadrate form in a
true epifaunal habit, this may not be correct.
The comparable byssus strength of similarly-
sized epibyssate arcaceans is much greater,
e.g. Bathyarca pectunculoides (Oliver &
Allen, 1980a), and consists of a single thick
stalk. The epibyssate limopsids may, there-
fore, require some degree of support and
could live in crevices or nestle at the base of
larger sedentary epifauna. Limopsis minuta
although normally taken from shell and coral
gravels, has also been recorded from muds.
These mud-dwelling species must be partially
infaunal and Oliver & Allen (1980b) noted that
some specimens did not develop the anterior
straight margin and remained in outline very
similar to L. aurita.

Glycymeriform group

The morphological features of classes M.C.
IX (App. Figs. 18 and 20) and M.C. X (App.
Fig. 21) are strongly convergent with those of
the Glycymeriaidae. From the morphological
features alone one could deduce the poor
shallow burrowing ability of these forms and
this is confirmed by the observations of Taylor
(personal communication) and Tevesz (1977)
(Figs. 5 and 6).

The anatomy of the foot is quite different
from those of the Limopsiform classes and
has only a very small toe and heel, being al-
together blade-like and very muscular. The
burrowing ability of this foot is aided by the
large posterior retractor. The dominance of
the posterior retractor is probably the cause of
the reduced condition of the anterior retractor
which has no or very little shell attachment.
This is identical in Glycymeris. Since valve
movements are important in burrowing, the
adductor and hinge are both stronger. The
former is evidenced in the reduced hetero-
myarian condition and the latter in the strong-
er hinge teeth which are set on a high arch. In
general, both classes tend towards an equi-
lateral outline; this too is a feature of the gly-
cymeridids. In both classes the shell is thick,
and this is necessary in arcoids not only to
develop strong hinge and muscle attach-
ments, but it is also needed to protect the ani-
mal when dislodged. Furthermore the thick
shell gives protection from crushing predators
(Vermeij, 1978).

Dislodgement is probably very common in
this group, as noted by Taylor (personal com-

munication) and may be one of the stronger
adaptive forces as it is for glycymeridids
(Thomas, 1975). Unlike glycymeridids, the
byssus remains functional, especially in M.C.
X. This suggests that this class is subject to
dislodgment and their occurrence on shell
hash supports the theory that the habitat is
subject to strong currents and consequent
disturbance. M.C. IX species possess a very
weak byssus by comparison, but they ap-
parently prefer sandy or muddy sand sub-
strates which are probably more stable. The
prominent ribbing on the M.C. IX species such
as Limopsis multistriata (Forskal, 1775) and
L. forteradiata (Cotton, 1931) may act to sta-
bilize the shell in these finer sediments.

The fixed sedentary burrowing mode con-
fines the inhalant and exhalant apertures to a
small area along the postero-ventral edge.
The strongly muscular mantle margin in this
region is capable of forming discrete aper-
tures and regulating the currents. The intake
of unwanted matter is, therefore, reduced and
the cleansing actions are required to a lesser
extent. This is reflected in the small amount of
gill axis muscle in these forms (App. Fig. 6B).
The periostracum, due to abrasion, is normal-
ly largely removed, but, if persistent, is only so
around the postero-ventral margin where it
still protects the current apertures.

Limopsis bassi Smith, 1885 (App. Fig. 19)
and L. eucosmus Verco, 1907 (App. Fig. 22)
represent intermediate forms between the
limopsiform and glycymeriform groups, L.
bassi being а М.С. IX associate and L.
eucosmus to M.C. X. Both tend towards a
more oblique form with a more advanced
heteromyarian condition and the foot has a
more strongly developed toe. The retractors,
hinge and other shell characters remain
glycymeriform. It is assumed that these inter-
mediates are less capable burrowers and
subsequently the extent of penetration is less.
Tevesz (1977), however, reports that L.
soboles (Iredale, 1931) behaves like L. loringi
and from examination of figures only there is a
similarity between the former species and L.
eucosmus. п Figs 5B and 6B the intermedi-
ates are shown as only semi-infaunal, but may
be able to completely burrow to the posterior
shell margin.

Abyssate group
The third group contains three classes

which are apparently not closely related
morphologically. They share an almost equi-

70 OLIVER

lateral outline, an almost isomyarian condition
and an apparent lack of byssus function.
These characters alone are sufficient to sug-
gest a shallow burrowing mode. Classes M.C.
XI (Limopsis vixornata Verco, 1907; App.
Figs. 23 and 25) and M.C. XII (L. brazieri
Angas, 1871; App. Fig. 26) share the slight
prosogyrate condition. The hinge, dorsally at-
tenuate shape, buttressed adductor and in-
ternally striate shell of L. vixornata cause it to
resemble the L. loringi (М.С. X) class. Ana-
tomically the foot and pedal retractors are
similar also. The greater equilateral form and
abyssate condition is, however, quite differ-
ent, but it is not unreasonable to assume that
L. vixornata represents an extension of the
glycymeriform burrowing type to a more ef-
ficient free burrowing type (Fig. 8). L. brazieri
with its elliptical outline probably represents
one extreme development of the burrowing
trend in the Limopsidae, but confirmation from
anatomical data is required. No habitat details
are available for either class but their sublit-
toral/shelf range and normal lack of perios-
tracum suggests that they inhabit sands or
coarser sediments.

Limopsis lilliei Smith (1885) (М.С. ХШ; App.
Figs. 24 and 27), although sharing the major
characters of this group, differs in possess-
ing a thin shell, covered by a pilose perios-
tracum, in the relatively weak hinge and the
complex ligament. The former differences can
be related to the soft muddy sediments pre-
ferred by this class in which dislodgment and
abrasion are likely to be less. The perios-
tracum is invariably clogged by sediment and
the fine erect hairs aid stabilization, through
preventing either sinking or dislodgment. The
weak hinge is unusual in burrowing limopsids,
but the well-developed secondary ligament
placed at the ends of the dorsal area are pre-
sumed to help in holding the valves together.
The intact lamellar layer is much larger than in
the ligament Types A-C. Combining the more
efficient ligament and the large equal ad-
ductors suggests that this class is made up of
relatively more efficient burrowers. It is ex-
pected that these forms would burrow up to
their postero-ventral margins (Fig. 7). The
mantle edge is especially thickened here and
could form precise inhalant and exhalant
openings. The gill axis musculature is almost
negligible and shows a further progression of
the condition seen in the glycymeriform
group.

EVOLUTION

The current extent of knowledge of the evo-
lution of the Limopsidae is poor due to the
limitations of the fossil record and lack of in-
vestigation. To examine all the available
material is beyond the scope of this paper and
reliance is placed mainly upon the published
data. The collection of Mesozoic limopsids in
the British Museum (Natural History) was ex-
amined.

Tevesz (1977) studied the problem of
limopsid origins, proposing a neotenous deri-
vation from the Grammatodontinae. Heinberg
(1976, 1978) extensively examined an as-
semblage of late Cretaceous (Maastrichtian)
limopsids; his study provides very significant
data on form and radiation. The functional in-
terpretations made by Heinberg (1979) do not
entirely agree with those in this paper and
consequently there are some revisions here.
Heinberg (1979) underestimates the extent of
endobyssate attachment and ploughing,
postulating either epifaunal or infaunal habits.
This study clearly shows that ploughing and
endobyssate habits in soft substrates are the
dominant limopsid life habits. Consequently,
the homeomorphs of the Recent compressed,
anteriorly reduced, heteromyarian forms are
not always epibyssate as suggested by Hein-
berg but many are semi-infaunal endobyssate
or ploughing species.

Cenozoic limopsids are more numerous but
there are apparently no studies concerned
with them alone.

Origins

Tevesz (1977) placed the origin of the
Limopsidae in the middle Jurassic (Bathon-
ian) citing Limopsis minima (Sowerby, 1825)
[= oolithica (Buvignier, 1852)] as the oldest
known species. Tevesz places great empha-
sis on the ligament pit as a limopsid character
and his interpretation rests strongly on its
presence. L. minima and L. oblonga (Sower-
by, 1825) are both well represented in the
BMNH collection. Contrary to the specific
name and small dimension of the type of
L. minima, it reaches a maximum size of
20 mm. It is sub-quadrate with slight posterior
extension, isomyarian and possesses a thick
shell with an impressed ligament area. In the
small species this ligament area resembles
that of a limopsid, but in some of the larger,

RECENT LIMOPSIDAE 71

better preserved specimens the area is
marked by oblique grooves and ridges (Fig.
9). This ridged ligament area is consistent
with the reduced duplivincular form seen in
grammatodonts. Oblique grooves are not
found in multivincular limopsid ligaments, any
ridging found being vertical. The form of the
juvenile ligaments in L. minima is typical of
most juvenile arcaceans and in itself is not
evolutionarily significant. There are no
grounds, therefore, for assigning L. minima to
the Limopsidae or for regarding this form as a
more probable limopsid ancestor than any
other grammatodont. A similar argument is
applicable to L. corallensis (Buvignier, 1852)
a late Jurassic species which has a distinct
duplivincular ligament.

Arkell (1929-1936) describes an unnamed
species from the late Jurassic (Oxfordian)
strata near Pickering, Yorkshire, England.
This species reaches 22 mm, is obliquely
circular, but the hinge is not preserved.

It is not until the lower Cretaceous (Albian)
that the first truly recognizable limopsid is
found. Limopsis albiensis (Woods, 1899) is
small—6 mm (Fig. 10A), obliquely circular,
heteromyarian with a smooth sculpture and a
small ligament pit. Overall it is an exact
homeomorph of juvenile Recent ploughing
species, e.g. L. aurita.

Although the exact origins of the Limopsidae
have not been elucidated, it is important to
note that whether L. sp. Pickering or Limopsis
albiensis represents the ancestral form; both
are obliquely circular. This indicates that the
ancestral life habit was semi-infaunal and
probably byssate.

Radiation

The initial trend is seen in two species
which occur in the Upper Albian, Limopsis
coemansi Briart & Cornet, 1868 (Fig. 10B)
and L. hoeninghausii (Muller, 1846) (Fig.
10C). L. coemansi is roundly oblique, oval
and rather tumid whereas L. hoeninghausii is
quadrate and tumid. These species show an
initial radiation into the endobyssate and
epibyssate modes.

Interpreting the shell character of Hein-
berg's (1979) species on the basis of the
anatomical data in this paper it is possible to
recognise the extent of the Late Cretaceous
(Maastrichtian) radiation. The Limopsiform
radiation is extensive: ploughing habits are

represented in Limopsis misjae Heinberg,
1976, endobyssate habits in L. ravni (Hein-
berg, 1976) and L. augustae (Heinberg, 1976).
The respective Recent conchological homeo-
morphs of these would be L. aurita, L.
oblonga and L. cristata and for both epi-
byssate species L. elachista. It is of note that
there are no large ploughing species in the
white chalk assemblage. The quadrate epi-
byssate species differ from Recent forms in
lacking any marginal crenulation.

Limopsis amandae (Heinberg, 1976) is
relatively tumid, but otherwise is typical of the
ploughing form. This tumidity, as Heinberg
notes, is indicative of an infaunal habit. How-
ever, given the strong heteromyarian condi-
tion of that species it seems doubtful whether
the adductor strength would be sufficient to
facilitate burrowing. A semi-infaunal habit is,
therefore, proposed for L. amandae.

Limopsis nanae (Heinberg, 1976) is a mi-
nute species (2.6mm). which possesses
peculiar sub-concentric ridges on the inner
shell margin. Heinberg postulates that the
size negates any requirement for anterior
reduction to facilitate epibyssate attachment.
However, L. nanae represents the juvenile
form of numerous limopsids which are not
necessarily epibyssate. Probably all limopsi-
form species are able to crawl and the small
size would aid this function (Tevesz, 1977)
giving L. nanae a broad niche. Heinberg at-
taches no significance to the marginal con-
centric ridges but they appear to be analog-
ous to the marginal ridge present in Nippono-
limopsis decussata (Adams, 1862) (=
nipponica Yokoyama, 1920) (Fig.12). М.
decussata has not been included in this paper
because, due to the presence of a prodisso-
conch cap (Fig. 11), it is considered to be a
philobryid. It was intended to make this ob-
servation the subject of a small paper, but it is
now useful to mention it here. This form of
margin is considered to be a valve locking
mechanism and is apparently unique to the
Limopsacea. The temptation to link Limopsis
nanae to N. decussata is strong and would
give added credence to Tevesz's (1977)
theory that the Philobryidae arose neotenous-
ly from the Limopsidae. The temporal and
spatial separation of the two species is so
large that such a link is doubtful, М. decussata
being known only from the Pleistocene of
Japan.

Limopsis helenae (Heinberg, 1976) has no

72 OLIVER

Recent homeomorphs and the epibyssate
habit is accepted.

The Glycymeriform radiation is also ap-
parent in the late Cretaceous (Newell, 1969)
in the form with radial ribbing. Heinberg’s
glycymeriform species Limopsis maggae
(Heinberg, 1978) is in contrast a smooth-
shelled form. In the northern hemisphere the
smooth-shelled forms are not apparent in the
Cenozoic, whereas the ribbed variety is fre-
quent, e.g. L. scalaris (Sowerby, 1825)
(Eocene). In the southern hemisphere there
are numerous smooth-shelled homeomorphs
of L. loringi and L. eucosmus occurring from
the Eocene onwards in the New Zealand and
Magellanic provinces (Fleming, 1966). From
the Cretaceous onwards there is an increase
in maximum size of both groups of glycymeri-
form limopsids.

The limopsiform groups display little further
radiation in the Cenozoic, the appearance of
large ploughing forms in Recent times being
the only event of significance. The epibyssate
species and fixed endobyssate species re-
mained small but did develop marginal
crenulations.

The isomyarian groups have poor fossil
records. М.С. XI (Limopsis vixornata) has a
probable homeomorph in the Palaeocene of
New Zealand, L. microps Finlay & Marwick,
1937 (Fleming, 1966). L. brazieri (М.С. XII)
has a very short fossil record, L. adamsiana
(Yokoyama, 1920) from the Pleistocene of
Japan is probably a homeomorph. М.С. XIII
(L. lilliei) has no fossil record and is presuma-
bly of relatively recent origin.

The fossil record of the limopsids is so
scant that the formulation of phylogenies can
only be hypothetical.

The origins of the family are not apparent
but if for the sake of discussion one follows
Stanley (1972), Tevesz (1977) and Morton
(1978) and invokes a neotenous derivation of
the Limopsacea, one must retain the Jurassic
arcacean ancestry. This ancestor, whether a
grammatodont or a cucullaeid, would pre-
sumably be isomyarian and retain the juvenile
arcoid ligament in a small triangular resilifer.
However, in the Limopsidae this ligament
when large becomes multivincular and lacks
chevrons. Furthermore the additions of new
ligament material are in lateral positions un-
like the central growth of the duplivincular
ligament. Therefore one must not simply as-
sign the limopsid’s origin to a neotenic event
but must also consider that the developmental
characteristics of the ligament have changed.

This change must now be interpreted in view
of Waller's (1978) classification of ligaments
in which he considers all Limopsacean liga-
ments to be duplivincular. Waller (1978) does
not indicate either ligament types B, C or D
and clearly there is much more work to be
done in this area before one can define the
significance of limopsid ligaments. In addition,
the initial radiation was towards the obliquely
oval heteromyarian condition which is unlike
all other arcoid tendencies as defined by
Stanley (1972). Stanley's repetitive neotenic
events consistently gave rise to trapezoidal
epibyssate forms or orbicular sub-trapezoidal,
shallow burrowing forms. The limopsid condi-
tion therefore represents a radical radiation
away from the arcoid plan and is only paral-
leled in the Arcacea by a few members of the
Striarcinae (Ovalarca) and Trinacriinae
(Stenzelia). Although the neotenous deriva-
tion of the Limopsids is not discounted here it
is felt that an oversimplification may be per-
petuated and it is urged that the Jurassic
arcoid radiation be reconsidered, especially
with regard to the almost simultaneous ap-
pearance of the Arcidae, Noetiidae and
Limopsidae.

The initial radiation of the Limopsiform
groups into epibyssate, endobyssate and
ploughing modes is well documented and has
followed the classic patterns defined by
Stanley (1972). The evolution of the ligament
types A, B and C within the limopsiform
groups is unclear. From the Recent forms
there appears to be little difference in the radi-
ation of those with Type A or C ligaments.
This suggests that the selective value may be
neutral and that these variations may have
existed for a long time. The presence of the
Type C ligament does, however, consistently
occur in those Recent species which also
possess crenulated margins. Such margins
are not observed in the early fossils and
therefore if the characters are linked there
may be a case for the Type С ligament being
secondary and forming a phyletic group. Con-
versely if the selective value of the Type C
ligament is neutral it may well have arisen al-
most at random throughout the evolution of
the limopsiform group.

The radiation into the glycymeriform and
abyssate burrowing modes is apparently sec-
ondary. This is quite certain in the glycymeri-
form group where their apearance in the late
Cretaceous and early Cenozoic is document-
ed. The retention of a heteromyarian condi-
tion testifies to this but it must be noted that in

RECENT LIMOPSIDAE 73

Limopsis loringi this condition is now slight.
This reversal can be equated with the “Case
|” evolution outlined by Stanley (1972) for
the endobyssate to free-burrowing sequences
seen in some of the Carditacea.

The radiation within the Glycymeriform
species has resulted in two distinct groups:
M.C. IX and M.C. X. Despite their similar
habits and morphologies there is no fossil
evidence to assume that they are part of a
single lineage. These groups could well rep-
resent convergence within the Limopsidae. If
so, this would indicate that such radiation oc-
curred at least once in the now antipodean
region and also in the now Mediterranean,
Caribbean Indo-Pacific region. This has re-
sulted in the distinct Recent distribution pat-
terns of the two classes.

The complete isomyarian conditions noted
in classes М.С. XI-M.C. XIII also appear to be
secondary. There appears to be reason to ac-
cept this for М.С. XI and М.С. XII as a con-
tinuance of the glycymeriform radiation pat-
tern. The fossil record is so scant that line-
ages are not considered. М.С. ХШ (Limopsis
lillie’), however, represents the appearance of
ligament type D, associated with rather non-
glycymeriform shell characters. п this class
there are no fossil homeomorphs known and
a gradual evolution of the Stanley Case Il
form seems untenable. This radiation may
well be attributable to yet another neotenous
event of the Case | type but associated with
ligament changes.

In conclusion, the limopsids rapidly reached
a peak in radiation by the early Cenozoic. This
was achieved from a semi-infaunal stock
radiating into the byssate modes to give rise
to the Limopsiform classes with reversals into
burrowing modes. These reversals may well
have been numerous and thus one sees no
evidence of a single lineage in the glycymeri-
form and abyssate burrowing groups. Coin-
ciding with the early Cenozoic peak there ap-
pears to be a high diversity of species with a
widespread shallow water distribution. This
situation declined gradually so that one now
sees the restrictive distributions and low spe-
cies diversity of recent Limopsidae.

LIMITING FACTORS IN THE MORPHO-
LOGICAL RADIATION, DIVERSITY AND
DISTRIBUTION OF LIMOPSIDS

Despite the functional radiation into plough-
ing, endobyssate, epibyssate, glycymeriform
and burrowing habits, the morphology of the

limopsids has remained remarkably con-
servative. The functional diversity has been
achieved through relatively small changes in
shell form and anatomy. The relatively high
functional diversity has, however, not been
paralleled by a high Recent species diversity,
there being at the most sixty valid species. Of
these, at least seventy percent are semi-
infaunal, either ploughing or endobyssate.
Only eleven percent are epibyssate, twelve
percent glycymeriform and eleven percent
non-glycymeriform burrowers. In comparison
with other Limopsacea there are at least eight
times as many glycymeridids as glycymeri-
form limopsids.

Distributionally, the limopsids are limited—
in the case of the limopsiform group, bathy-
metrically and the burrowing groups, geo-
graphically.

In the Atlantic Ocean the limopsiform spe-
cies are found almost exclusively from the
continental margin zone to the abyss, and
never occur in shallow shelf waters. Excep-
tions to this are few; some polar emergence
occurs in Norwegian fjords and the epi-
byssate quadrate Limopsis antillensis occurs
in relatively shallow waters in the Caribbean.
The Japanese zonation (Okutani, 1968) is
similar, although the outer shelf is inhabited
by some species. Only in the Antarctic do
limopsiform species occur widely on the shelf
(Dell, 1964). In general, the Limopsiform spe-
cies are restricted to cold water and normally
do not occur on the shelf.

The ribbed glycymeriform class is not deep
water and occurs from the littoral to 400 m.
This class is, however, geographically re-
stricted to the Indo-Pacific and Mediterranean
(Coen, 1931). The smooth-shelled glycymeri-
form class is restricted to the shelf and con-
tinental margin zone and is endemic to south-
east Australia. The non-glycymeriform bur-
rowing classes are similarly restricted geo-
graphically, two classes being endemic to
southeast Australia and the third to Antarc-
tica.

The Limopsidae with their restricted
morphological diversity and distributional limi-
tations could be considered a relatively un-
successful family especially in their degree of
attainment of the epibyssate and burrowing
habits. The semi-infaunal forms are more
numerous but in a life mode which has been
abandoned by the majority of the Recent bi-
valves. The mechanism and extent of these
limitations warrant further analysis for each
major functional group.

74 OLIVER

The glycymeriform limopsids represent the
initial radiation into the burrowing habit. This
occurred very soon after the appearance of
the Glycymerididae (Aptian/Albian). How-
ever, despite this almost equal time scale,
there is a marked contrast in the relative suc-
cess of the two groups.

Thomas (1976) showed the glycymeridid
duplivincular ligament to be too weak to en-
able efficient burrowing and with the result
that the animals were subject to repeated dis-
lodgment. They are therefore not only adapt-
ed to survive the subsequent physical and
predation pressures, but also to rapidly re-
establish themselves in the substrate. The
shells are consequently large, thick and orbic-
ular with a strong hinge. As there is consider-
able convergence between the two groups,
one can expect similar limitations to operate.
The weakness of the glycymeridid ligament
involves a combination of an inherent struc-
tural frailty with allometric growth. The
strength of the limopsid alivincular ligament
could not be measured as no live specimens
were available. The glycymeriform limopsid
ligament (Type A) is always formed in a very
shallow resilifer and one never observes the
deep resilia seen in Ostrea or Vulsella. This
shallow ligament area is reminiscent of the
typical arcoid structures and may well not
possess the qualities of non-arcoid types. It is
assumed here that the limopsid ligament is no
more efficient than the duplivincular, especial-
ly with regard to their similarities in length of
attachment, thickness of non-split layers and
degree of umbonal growth. Allometric rela-
tionships between the ligament and shell of
limopsids can be shown. In two ploughing
species, Limopsis aurita and L. marionensis,
results for mean log-log reduced major axis
regressions indicated allometric relationships
of ligament height, length and area with shell
height. Results for L. aurita ligament areas
were a correlation coefficient of 0.94 and a
slope of 3.09 where a slope of 2 would be
considered isometric for a linear-area rela-
tionship. Results for ligament heights and
lengths separately were for L. aurita: liga-
ment height r = 0.93, slope 1.54; ligament
length r = 0.94, slope 1.58 and for L.
marionensis: ligament height r = 0.95, slope
= 1.35; ligament length r = 0.96, slope =
1.57. In these results the parameters are both
linear and have an expected slope of 1.0 for
an isometric relationship. The consequences
of allometric growth are rapid dorsal splitting
of the ligament (Trueman, 1969) and the re-

sulting ventral growth which interferes with
the hinge. In glycymeridids the replacement is
central but in large limopsids where the liga-
ment becomes multivincular, replacement is
also in lateral sites. Consequently, ventral
encroachment is more widespread in the
limopsids, so much so that in some large
specimens (60mm) of L. marionensis, no
well-formed hinge teeth remain. Glycy-
meridids, however, may attain a much greater
size (120 mm) without such severe tooth loss.
It is noted that in glycymeriform limopsids
multivincular structures are never developed
and this may reflect the need to maintain a
strong hinge. Furthermore, the multivincular
ligament involves considerable elongation of
the dorsal area with consequent changes in
shell outline. This has been classically shown
in Perna (Trueman, 1954) but is also true to a
lesser extent here as evidenced in the onto-
genetic changes seen in L. tenella (Oliver &
Allen, 1980b) and L. marionensis. Such
changes in outline would severely impair the
burrowing ability of glycymeriform limopsids.

In these limopsids most growth is ventral
and thus one observes deeply cleft dorsal
areas and dorsally attenuated forms. This de-
velopmental restriction may therefore account
for the small size of glycymeriform limopsids.
This in itself may be disadvantageous as the
smaller shells may be more prone to attack by
crushing predators, a situation which (Vermeij,
1978) may contribute to the limited success of
the limopsids in shallow water.

An additional disadvantage inherent in the
glycymeriform limopsids is their derivation
from a heteromyarian stock. Although this
condition is reduced in recent forms there
must be restrictions to burrowing caused by
the weakness of the anterior adductor and the
unequal forces created by this condition. The
glycymeridids arose as an isomyarian group
and have thus not been influenced in this
manner.

The few isomyarian burrowing limopsids
that exist are small forms. Limopsis brazieri
and L. vixornata have a structural affinity with
the glycymeriform group and are therefore be-
lieved to be subject to the same adaptive re-
strictions. Despite the isomyarian condition of
these groups, their diversity and distribution is
more limited than that of the glycymeriform
group. This adds more credence to the hy-
pothesis that the ligament structure is the
major adaptive restriction. The Antarctic iso-
myarian group is, in contrast, widespread in
its endemic province and also occurs in large

RECENT LIMOPSIDAE 75

numbers to the extent that they may be the
dominant bivalve in many samples. These
species, e.g. L. /illiei, contrast morphological-
ly in possessing a weak, thin shell with a weak
hinge. Considerable ventral encroachment
occurs in these forms and an edentulous
space is rapidly developed, restricting the
number of teeth to 3—5 on either side. The
alivincular ligament is proportionately large
and may be aided by the secondary ligament
areas on the dorsal areas. These secondary
areas may also strengthen the hinge as they
lie immediately above the remaining hinge
teeth. It has already been argued that such a
thin-shelled, weak-hinged form is not viable
and that the limopsid ligament is incapable of
providing the mechanism for efficient burrow-
ing. But here is an apparently successful bur-
rowing limopsid. Mechanics alone cannot ex-
plain this anomaly. An examination of the
Antarctic fauna highlights some contrasting
competitive pressures experienced by non-
siphonate, shallow burrowers. The Antarctic
bivalve fauna has a unique make-up and has
few siphonate suspension feeders (Powell,
1960; Dell, 1964). Furthermore, the diversity
of non-siphonate burrowers is not as high as
in temperate or tropical regions. It is probable,
therefore, that the inefficient burrowing
limopsids are subject to less competitive
pressure in the Antarctic province. The Ant-
arctic is unusual in that the fauna as a whole
is impoverished and in particular lacks any
benthic decapod Crustacea (Vermeij, 1978).
Following Vermeij (1978) it can be argued
that the lack of crushing predators has not
necessitated the evolution of heavy, strong-
hinged shells. Consequently ligament en-
croachment on the hinge in L. /i/liei would not
be too disadvantageous in relation to preda-
tion. Allometric ligament growth could then
proceed, creating a stronger ligament for
more efficient burrowing.

In comparison with other bivalve groups,
the limopsiform classes are poorly adapted.
The endobyssate class has not paralleled the
Modiolidae, Pinnacea or Pteriacea and a
similar condition occurs between the epi-
byssate class and the Mytilidae and Arcidae.
The semi-infaunal classes do have analogues
in the Palaeozoic, represented by some
members of the Cyrtodontidae, Inocerami-
dae, Modiomorphacea and Carditacea, but
few in the Recent. Stanley (1972) discusses
the Palaeozoic and Mesozoic decline of the
semi-infaunal bivalve and its replacement by
highly adapted infaunal burrowing forms. A

consequence of this decline was the emerg-
ence of the epibyssate bivalves during the late
Palaeozoic and Mesozoic.

In the Mesozoic there must have been con-
siderable adaptive pressure to radiate into the
two highly adapted life modes of burrowing
and epibyssate attachment. The Limopsidae,
arising as semi-infaunal species, rapidly re-
sponded to this pressure, reaching their peak
as represented by the monomyarian Limopsis
augustae in the late Cretaceous. From this
point the epibyssate and endobyssate limop-
sid radiation remained static and the highly
adapted byssate forms were never paralleled.
Apparently unable to adapt further, the limop-
sids were at a considerable disadvantage and
could not compete with the now dominant ad-
vanced byssate forms. Consequently the
limopsiform classes were restricted to zones
of higher stability and less competition—thus
their deep water bathymetric range and oc-
currence in the low diversity, highly endemic
Antarctic fauna. This limitation is very close to
that experienced by the Brachiopoda and, at
least in the Atlantic and Antarctic, the co-
occurrence of limopsids and brachiopods is
high (personal observations).

The mechanism preventing further limopsid
radiation into the epibyssate and endobyssate
habits is probably a function of the degree of
anterior reduction. The extent of anterior re-
duction in the Arcacea is limited by the func-
tional and growth constraints of the duplivin-
cular ligament (Thomas, 1978a, 1978b). As
limopsids possess an alivincular ligament this
mechanism may at first not appear to be rele-
vant, a view which was supported by Hein-
berg (1979).

Anterior reduction in limopsids necessitates
reduction of the hinge teeth and dorsal area.
In mytiliform bivalves this is of little conse-
quence as the ligament is strong enough to
hold the valves together and to articulate
them. The limopsid alivincular ligament is
restricted to a very shallow triangular resilifer
displaced on the dorsal area and is, therefore,
not suited to maintain valve adhesion without
hinge teeth. However, the Philobryidae, which
accepting Tevesz (1977) and Morton (1978)
are derived from Limopsidae, have succeed-
ed in radiating into edentulous mytilid homeo-
morphs via a progression from the limopsid-
like genus Cratis to Cosa to Philobrya. The
significant feature of epibyssate radiation in
both the Limopsidae and Philobryidae is the
universal small size of the shells. This sug-
gests that the edentulous, anteriorly re-

76 OLIVER

duced form is attainable only through minia-
turization and this leads one to consider again
the growth characteristics of limopsids. Com-
bining the effects of the anterior reduction on
the size of the dorsal area and number of
hinge teeth with the allometric ligament, it is
observed that the two are mutually exclusive.
As anterior reduction diminishes the size of
the dorsal area, it reduces the potential size of
the ligament. In very small species this effect
is negligible. However, as the linear dimen-
sion of the shell increases, the limitation of the
ligament size is rapidly increased, the coun-
teracting forces soon preventing further
growth.

The limitations of the limopsid radiation,
their recent diversity and distribution therefore
appear to be a function of inherent morpho-
logical constraints. These constraints are pri-
marily the inefficient alivincular ligament and
the lack of any siphonal development. Some
minor evolutionary events such as the initial
heteromyarian condition may have contrib-
uted to the limitation of the family. However,
competitive and predation pressures have
also played a modifying role. These in general
have been restrictive, resulting in the absence
of semi-infaunal species from shelf waters
and the further restriction of burrowing spe-
cies. In the case of the Antarctic, such pres-
sures are reduced and one observes a more
diverse and prominent limopsid element in the
fauna.

ACKNOWLEDGEMENTS

| thank Roger D. K. Thomas for his very
helpful comments on the manuscript of this
paper. Among many others who aided with
advice and specimens were S. Whybrow, N.
J. Morris, D. Heppell, K. Boss, H. Coomans,
B. Metivier, R. Kilburn, W. Ponder and T.
Habe.

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KEY TO ABBREVIATIONS USED IN
APPENDIX ANATOMICAL FIGURES

A Anus

AA Anterior adductor muscle
Anterior retractor muscle
B Byssus

Byssus retractor element
Byssus retractor muscle
Cr Connective tissue

DG Digestive gland

F Foot

G Gill

GD Gonad

GA Gill axis

САМ Gill axis muscle
H Heart

HG Hind gut

K Kidney

KD Kidney duct

ME Mantle edge

MN Mantle nerve

Р Palps

PA Posterior adductor muscle
PPM Pedal protractor muscle
РАМ Posterior retractor muscle

APPENDIX: MORPHOLOGICAL CLASSES
OF RECENT LIMOPSIDS

To present all the morphological data on
fifty species would be confusing and conse-
quently the species have been divided into
classes of similar morphology. These classes
cannot be rigidly defined and therefore there
are some intermediate species. These are
described separately only if they provide sig-
nificant additional data. There are thirteen
distinct classes which require definitions. The
descriptions have been confined to concise
diagnoses, using only characters of functional
significance.

Some of the shell characters of the Limop-
sidae have not been adequately defined be-
fore. This has not only given rise to the con-

RECENT LIMOPSIDAE 79

if e
at” tl! dl M и». “o
M ‘

th |
N

LIGAMENT TYPE A

Dorsal Area

Secondary
ligament

APP. FIG. 1. Ligament structures within the Limopsidae.

fused state of limopsid systematics, but has
also obscured functional interpretation.
Ligament: The ligament in the limopsids,
although typically alivincular (Trueman, 1969),
is not always of the simple amphidetic type.
There are four distinct forms (Oliver, in prep.)
in which the disposition of the fibrous and
lamellar layers differ; there is also a second-
ary ligament in some. The nature of the sec-
ondary ligament is uncertain and at this mo-
ment it is not known whether it is periostracal
or a fusion layer. Туре A.—Amphidetic
alivincular: Primary ligament in a shallow
resilifer, remainder of dorsal area covered by
undifferentiated periostracum (App. Fig. 1).
Type B.—Amphidetic multivincular: Primary
ligament of multiple lamellar and fibrous seg-
ments all in shallow resilifer, remainder of
dorsal area covered by undifferentiated
periostracum (App. Fig. 1). TYPE C.—Pri-
mary ligament of fibrous layer only in a rela-
tively deep and narrow resilifer. Dorsal area

covered by a thick layer of presumed second-
ary ligament joining the whole length of the
dorsal area. The dorsal area may, however,
be covered by the lamellar layer (App. Fig. 1).
Type D.—Primary ligament of the amphidetic
alivincular form (Type A). Dorsal area covered
with a secondary ligament which is especially
thickened at the ends of the hinge plate (App.
Fig: uh):

Marginal crenulations: Type A.—Nodu-
lar, margin marked by alternating nodules and
pits or ridges and troughs. Distinguishing
ridges and nodules are impractical due to
ontogenetic changes from one to the other.
Type B.—Serrated, margin smooth except for
fine serrations on its inner edge. This type is
probably formed from Type A by overgrowth
as the shell increases in size. Type C.—Flut-
ed, the inner margin is more or less smooth
except for weak undulations or corrugation
which coincide with the radial ribs of the ex-
ternal sculpture.

80 OLIVER

APP. FIG. 2. Limopsis marionensis Smith. Baie de Penguins, Antarctica. IRSNB. Diam. 65 mm. APP. FIG. 3.
Limopsis chuni Thiele & Jaeckel. Natal, South Africa. NM. Diam. 30 mm. APP. FIG. 4. Limopsis vaginata
Dall. Bering Sea. IRSNB. Diam. 35 mm.

Periostracal bristles: Thatched.—Long
fine bristles lying flat against the shell and
forming a wide fringe. Spicate.—Short blade-
like bristles standing more or less erect and
not forming a wide fringe. Lanceolate.—Long
needle-like bristles standing more or less
erect and not forming a wide fringe. Stub-
bly.—Short blunt coarse bristles standing

erect from shell. Pilose.—Moderately long
very fine bristles, dense, standing erect.

Morphological Class |
Diagnosis: Larger species 20-60 mm max.

diam. Equivalve, compressed, inequilateral,
becoming obliquely oval or obliquely circular,

RECENT LIMOPSIDAE 81

APP. FIG. 5. Gross anatomy of Limopsis marionensis Smith (left mantle removed).

i.e. strongly extended posteriorly. Shell thin.
Sculpture weak, of concentric lines cut by
radially arranged markings corresponding to
periostracal bristle insertions. Periostracum
thatched. Ligament (Type A) variable, becom-
ing large or multivincular (Type B) in big spec-
imens of large species. Dorsal area typically
long, narrow and not deeply cleft, but may
widen disproportionately. Hinge weak with
numerous small teeth set in two series on a
low arch, an edentulous space of variable size
is present. Heteromyarian condition ad-
vanced, the anterior adductor is reduced and
possesses a weak scar-umbonal ridge
(myophore). Internal margin smooth (App.
Fig. 2).

Foot with prominent toe and heel. Pedal re-
tractors not large. Byssus gland active, pro-
ducing a single long fine thread without any
terminal disc. The byssus is rarely observed
and is usual only in juveniles. Gill axis orien-
tated obliquely to the hinge plate, highly
muscular. Palps small with few weak sorting
ridges. Mantle margin thickened postero-
ventrally but not greatly (App. Figs. 5 and 6).

Habitat: Typically from sands, muds and
oozes, but also from gravels.

Bathymetric range: 50-5500 т.

Distribution: cosmopolitan, but absent from
the Arctic Ocean.

Species complement: Limopsis marionen-
sis Smith, 1885; L. tajimae Sowerby, 1914; L.
dalli Knudsen, 1970; L. tenella Jeffreys, 1876
(= pelagica Smith, 1885); L. ruizana Rehder,
1971; L. surinamensis Oliver & Allen, 1980b;
L. zonalis Dall, 1908.

Tentatively included are Limopsis janeiro-
ensis Smith, 1915; L. indica Smith, 1885; L.
siberutensis Thiele & Jaeckel, 1931 and L.
paradoxa (Iredale, 1931).

Morphological Class Il

Diagnosis: Like M.C. | except that the sculp-
ture is stronger and the periostracum a little
coarser. Inner margin serrated. Ligament
Type C. Anatomy essentially as in M.C. |
(App. Fig. 3).

Habitat: Sands and muds.

Bathymetric range: 70-500 m.

Distribution: Indian Ocean (East and South
Africa) and Korean Sea.

Species complement: Limopsis спит
Thiele & Jaeckel, 1931; L. sansibarica Thiele
& Jaeckel, 1931; L. belcheri (Adams &
Reeve, 1850).

82 OLIVER

APP. FIG. 6. Transverse sections through the region of the heart to show comparative extent of the gill axis
musculature. (A) Limopsis tenella (Limopsiform). (В) L. multistriata (Glycymeriform). (С) L.lillei (Burrowing).

Morphological Class Ill

Diagnosis: Like M.C. | except for the pres-
ence of a cleft formed by an indentation of the
postero-dorsal shell margin. The cleft appears
in juveniles as a small notch below the end of
the dorsal area and increases in size with
growth. There is a much smaller anterior cleft

in Limopsis cumingi. Ligament Type A. Ana-

tomically similar to M.C. | (App. Figs. 4 and 7).
Habitat: Fine sands and muds.
Bathymetric range: 80-650 m.
Distribution: North Pacific (Alaska-Japan).
Species complement: Limopsis vaginata

Dall, 1891; L. cumingi A. Adams, 1862.

RECENT LIMOPSIDAE 83

APP. FIG. 7. Growth series of Limopsis cumingi A.

Adams to show development of the clefts.

Morphological Class IV

Diagnosis: Medium-sized species: diam.
12-20 mm. Compressed, becoming strongly
and obliquely oval. Periostracum thatched.
Shell moderately thick. Ligament Type A.
Hinge moderately strong, teeth larger than
those in M.C. |. Heteromyarian condition ad-
vanced, greatly reduced anterior scar with
well developed myophore. Anatomy as in М.С.
| except that the posterior pedal retractor is
slightly divided into byssus and pedal ele-
ments, the former being far the weaker.
Byssus of a single long fine thread which is
frequently observed (App. Figs. 8 and 11).

Habitat: Muddy gravels, shell gravels,
sands and muds.

Bathymetric range: 100-1300 т.
Distribution: Atlantic Ocean and Japan.
Species complement: Limopsis aurita

(Brocchi, 1814); L. sulcata Verrill & Bush,

1898; L. obliqua A. Adams, 1862.

Some of the smaller species included in
M.C. | may belong here but the anatomical
characters are not known, e.g. Limopsis
indica, L. janeiroensis..

Habits: The following behaviours of Limop-
sis aurita were observed by Oliver & Allen
(1980b):

In mud: L. aurita ploughs through the sedi-
ment surface penetrating only to a depth
marked by a line through the umbos and
postero-ventral margin. No burrowing move-
ments were observed. When ploughing

ceased, most specimens remained in an up-
right position and produced the fine byssus
(App. Fig. 12).

In sand: A similar behaviour occurs, but
penetration is much less and the byssus is not
able to prevent the animals from falling onto
one valve (App. Fig. 12).

On gravel: The crawling persists, but no
penetration is effected and the byssus is ce-
mented to stones. In many cases the animals
suspended themselves from larger stones
hanging freely in the water (App. Fig. 12).

Morphological Class V

Diagnosis: Small species: diam. 5-12 mm.
Compressed, inequilateral, becoming ob-
liquely oval, occasionally obliquely circular,
some developing a straight anterior margin.
Shell thin, sculpture weakly decussate. Peri-
ostracal bristles stout, lanceolate or spicate,
arranged in distinct radial or concentric pat-
terns, persistent especially postero-ventrally.
Ligament Туре С. Hinge weak, teeth small on
a low arch. Heteromyarian condition ad-
vanced, small anterior scar with weak myo-
phore. Internal margin evenly crenulated,
nodular. Anatomically similar to M.C. IV but
the divided posterior pedal retractor has a
stronger byssus element. The byssus con-
sists of 3-6 long fine threads. Mantle margin
thickened postero-ventrally (App. Figs. 9 and
13).

Habitat: Sands, muds and oozes.

Bathymetric range: 50-2500 m.

Distribution: Cosmopolitan except for the
Arctic Ocean.

Species complement: Limopsis affinis,
Verrill, 1885; L. cristata Jeffreys, 1876; L.
erecta Hedley & Petterd, 1906; L. idonea
(Iredale, 1931); L. intermedia Oliver & Allen,
19806; L. longipilosa Pelseneer, 1903; L.
perieri Fischer, 1870; L. scabra Thiele, 1912:
L. spicata Oliver & Allen, 1980b; L. lanceolata
Oliver & Allen, 1980b; L. tasmani (Dell, 1956).

The following species are tentatively in-
cluded: L. diazi Dall, 1908; L. mabillana Dall,
1908 and L. stimpsoni Dall, 1908.

Limopsis diegensis Dall, 1908 (App. Figs. 10
and 13)

This species closely resembles M.C. V
species both in shell and anatomy. It is larger,
reaching 15mm in diam. and possesses a
‘thatched’ periostracum. It is obliquely circular
rather than obliquely oval.

84 OLIVER

APP. FIG. 8. Limopsis aurita Brocchi. Bay of Biscay. MNHNP. Diam. 15 mm. APP. FIG. 9. Limopsis affinis
Verrill. Off New England, U.S.A. USNM. Diam. 10 mm. APP. FIG. 10. Limopsis diegensis Dall. Off California.

USNM. Diam. 12.5 mm.

Limopsis oblonga A. Adams, 1860 (App. Fig. Juveniles have a concentric spicate perios-

14) tracum, but the adults are more of the
‘thatched’ type.
This is another species with an evenly Habitat: Sands and muds.
crenulate margin and a somewhat spicate Bathymetric range: 100-2020 т.
periostracum. It is, however, larger, reaching Distribution: Japan.

15 mm in diam. and is relatively a little tumid.

RECENT LIMOPSIDAE

APP. FIG. 11. Gross anatomy of Limopsis aurita Brocchi (left mantle lobe removed).

APP. FIG. 12. Life positions of Limopsis aurita in A gravel, B sand and C mud.

86 OLIVER

y ©
y S52
e

APP. FIG. 13. Gross anatomy of Limopsis diegensis Dall (left mantle lobe removed). This anatomy is typical

of all M.C. V forms.

Morphological Class VI

Diagnosis: Small species: diam. 6 mm.
Relatively slightly tumid, inequilateral, becom-
ing slightly obliquely oval. Sculpture weak.
Periostracum pilose, of dense short stubbly
bristles, not fringing. Heteromyarian condition
slight. Hinge moderately strong but consisting
of few teeth. Ligament small, Type C. Inner
margin crenulate and nodular. Anatomically
similar to M.C. V, but showing a suite of
abyssal adaptations (Oliver & Allen, 1980b).
Byssus of 3-5 slender, long, fine threads.

Habitat: Ooze.

Bathymetric range: 3500-5500 m

Distribution: Atlantic Ocean.

Species complement: Limopsis galathea
Knudsen, 1970.

Two abyssal Pacific species have shell
similarities to Limopsis galathea but anatomi-
cal data are not available to substantiate this
overall similarity. The species are L.
panamensis Dall, 1908 and L. juarezi Dall,
1908.

Morphological Class VII

Diagnosis: Small species reaching 15 mm
diam. Relatively tumid, inequilateral, becom-
ing markedly obliquely oval with a tendency to
develop a short straight antero-dorsal margin.
This development may not always occur.
Shell relatively thick. Hinge reduced anterior-
ly, but teeth relatively large. Ligament Type A.
Heteromyarian condition extreme, the minute
anterior adductor with a prominent myophore.
Inner margin crenulate, evenly nodular in
juveniles, in adults reduced to 3-5 strong
postero-ventral ridges. Anatomically similar to
M.C. IV, but the byssus element of the poste-
rior retractor is large and not attached to the
shell but inserted into the posterior adductor.
The toe of the foot is bulbous and the byssus
gland is large. The byssus consists of a
sheath with 4—6 short strap-like threads (App.
Figs. 15 and 17).

Habitat: Gravels, shell and coral hash, oc-
casionally on finer sediments.

Bathymetric range: 50-2500 т.

RECENT LIMOPSIDAE 87

4
‘
it}
Le
+
4
$

APP. FIG. 14. Limopsis oblonga A. Adams. Sagami Bay, Japan. RSM. Diam. 14 mm. APP. FIG. 15.
Limopsis minuta Philippi. Bay of Biscay. MNHNP. Diam. 12 mm. APP. FIG. 16. Limopsis natalis Barnard. Off

Natal. NM. Diam. 4 mm.

88 OLIVER

APP. FIG. 17. Gross anatomy of Limopsis minuta Philippi (left mantle lobe removed).

APP. FIG. 18. Limopsis multistriata (Forskal). Off Kenya. MCZ. Diam. 25 mm. APP. FIG. 19. Limopsis bassi
Smith. South Australia. SAM. Diam. 25 mm.

RECENT LIMOPSIDAE 89

APP. FIG. 20. Gross anatomy of Limopsis multistriata (left mantle lobe removed).

Distribution: Atlantic Ocean.

Species complement: Limopsis minuta
(Philippi, 1836) and L. abyssicola A. Adams,
1862.

The New Zealand species Limopsis lata
Smith, 1885 has a similar shell morphology
but no confirmatory anatomical details are
available.

Morphological Class VIII

Diagnosis: Minute species rarely exceeding
diam. of 5mm, relatively tumid, becoming
obliquely quadrate with a long straight antero-
dorsal margin. Sculpture weakly decussate.
Periostracum ‘thatched.’ Ligament small,
Type C. Dorsal area small. Hinge reduced
anteriorly with few but relatively large teeth.
Heteromyarian condition extremely ad-
vanced. Anterior myophore small. Margin
crenulated as т М.С. VII except that the pos-
tero-ventral emphasis is present in all but the
smallest specimens. Anatomically similar to
М.С. VII but there is no specialized byssus

retractor. Byssus consists of 3—5 short strap-
like strands (App. Fig. 16).
Habitat: Sands and shell gravels.
Bathymetric range: 100-600 т.
Distribution: Caribbean and Southeast
Africa.
Species complement: Limopsis antillensis
Dall, 1881; L. natalis Barnard, 1964 and L.
elachista Sturany, 1899.

Morphological Class IX

Diagnosis: Moderately large species: diam.
25-45 mm. Equivalve, compressed, becom-
ing obliquely circular, some large specimens
dorsally attenuate. Shell thick. Sculpture of
both concentric and radial ridges, more or
less decussate in juveniles but radially ribbed
in adults. Periostracum ‘thatched,’ but not
persistent except at the postero-ventral mar-
gin. Dorsal area variable, usually small and
narrow, but in dorsally attenuate species this
area is expanded, remaining deeply cleft. Lig-
ament Type A, variable and may be large.

90 OLIVER

APP. FIG. 21. Limopsis loringi Angas. Port Stephen, New South Wales. AMS. Diam. 33 mm. APP. FIG. 22.
Limopsis eucosmus Verco. Gt. Australian Bight. SAM. Diam. 21 mm.

Hinge strong, teeth numerous, in two distinct
series set on a high arch, central teeth of each
set are the largest. Heteromyarian condition
slight, both scars with fine buttresses. Shell
between scars evenly radially striate. Inner
margin crenulated, fluted. Foot with reduced
toe and heel, blade-like, highly muscular.
Posterior pedal retractors simple, large. Ante-
rior dorsal retractors spread over the visceral
mass with little or no shell attachment. Byssus
gland small but capable of producing a single
long fine thread which is, however, rarely ob-
served. Gill axis orientated vertically relative
to the hinge plate; axis musculature very
small. Palps with numerous well-developed
sorting ridges. Mantle edge greatly thickened
postero-ventrally (App. Figs. 6B, 18 and 20).

Habitat: Sands, silts and muds.

Bathymetric range: 0-400 m.

Distribution: Indo-Pacific and South Aus-
tralia.

Species complement: Limopsis multistriata
(Forskal, 1775); L. compressa G. & H. Nevill,
1874; L. cancellata (Reeve, 1843); L. wood-
wardi A. Adams, 1862; L. macgillivrayi A.
Adams, 1862; L. torresi Smith, 1885; L.
Japonica A. Adams, 1862; L. forskali A.
Adams, 1862; L. soyoae (Habe, 1953); L.
tenisoni T. Woods, 1877; L. tenuiradiata Cot-
ton, 1931; L. forteradiata Cotton, 1931.

Habits: J. D. Taylor (personal communica-
tion) has observed Limopsis multistriata living
in sub-littoral sands off Shimoni, Kenya. They
were observed to burrow completely in the
sand although a number were lying free on
the surface.

Limopsis bassi Smith, 1885
This species is similar to M.C. IX species,

but is obliquely oval with a less rounded an-
terior margin. The sculpture is weaker, as is

RECENT LIMOPSIDAE 91

APP. FIG. 23. Limopsis vixornata Verco. Neptune Island. South Australia. SAM. Diam. 10 mm. APP. FIG. 24.
Limopsis lilliei Smith. South Orkney Islands, Antarctica. NMW. Diam. 14 mm.

GA
(remains of

APP. FIG. 25. Gross anatomy of Limopsis vixornata Verco.

= OLIVER

APP. FIG. 27. Gross anatomy of Limopsis lilliei Smith (left mantle lobe removed).

the hinge. The heteromyarian condition is
greater, similar to that of М.С. I. The foot has a
well-developed toe. The antero-dorsal retrac-
tors have shell attachments. The gill axis is
orientated obliquely (App. Fig. 19).

Habitat: Sands.

Bathymetric range: Shelf zone.

Distribution: South Australia.

Morphological Class X

Diagnosis: Very similar to M.C. IX, but the
sculpture is very finely decussate and the
inner margin is smooth. Tevesz (1977) shows
the anatomy to be similar to that of M.C. IX in
the form of the foot and orientation of the gill
axis. The byssus differs in being active, pro-

RECENT LIMOPSIDAE 93

ducing up to five long fine threads (App. Fig.
ait):

Habitat: Shell hash.

Bathymetric range: 40-70 т.

Distribution: Southeast Australia.

Species complement: Limopsis loringi
Angas, 1873; L. soboles (lredale, 1931) and
L. dannevigi (lredale, 1931).

Habits: Tevesz (1977) described the bur-
rowing actions of Limopsis loringi and L.
soboles. Burrowing action is slow, taking up
to 45 mins to burrow completely up to the
postero-ventral margin. No indication of
ploughing activity was given by Tevesz.

Limopsis eucosmus Verco, 1907 (App. Fig.
22)

This is a South Australian species which is
similar in outline and anatomy to L. bassi, i.e.
it is a heteromyarian oblique form with a toed
foot. Its other shell characters are, however,
of the M.C. X form. The variety penelevis
Verco, 1907 is even more extreme in its thin-
ner shelled compressed form. The character
of the byssus is not known; the byssus slit is
well developed.

Morphological Class XI

Diagnosis: Small species reaching 12 mm
in diam. Equivalve, compressed, almost in-
equilateral, sub-circular with a slight posterior
extension, large specimens dorsally attenu-
ate. Umbos very slightly prosogyre. Shell
moderately thick. Sculpture concentric with
very weak radial markings. Periostracum
‘thatched’ but not persistent. Dorsal area
small, narrow. Ligament small, Type A. Hinge
moderate, teeth in two series on a moderate
arch, central teeth in each set dominant. Ad-
ductor scars sub-equal, heteromyarian condi-
tion slight, both scars weakly buttressed.
Margin smooth. Examination of dried soft
parts showed some critical features. Foot
bladelike with small heel and toe. Posterior
pedal retractors large. Anterior retractor with
little or no shell attachment. The dried trans-
lucent foot showed no trace of the dark stain-
ing typical of the byssus gland. No byssus slit
was observed. Mantle edge greatly thickened
(App. Figs. 23 and 25).

Habitat: Unknown.

Bathymetric range: 70-200 т.

Distribution: South Australia.

Species complement: Limopsis vixornata
Verco, 1907 and L. occidentalis Verco, 1907.

Morphological Class XII

Diagnosis: Small shells reaching 7 mm in
diam. Equivalve, relatively slightly tumid, sub-
equilateral with slight posterior extension,
longer than high; sub-elliptical. Umbos proso-
gyre. Shell thick. Sculpture concentric with
very weak radial markings. Dorsal area short,
ligament relatively large Туре A. Hinge mod-
erately strong but with few teeth. Hetero-
myarian condition slight, adductor scars sub-
equal, both buttressed. Margin smooth. No
anatomical details available (App. Fig. 26).

Habitat: Unknown.

Bathymeric range: Shallow shelf zone.

Distribution: New South Wales, Australia.

Species complement: Limopsis brazieri
Angas, 1871.

Morphological Class XIII

Diagnosis: Medium-sized species: diam.
20-25 mm. Equivalve, relatively slightly tumid,
sub-equilateral, very slightly posteriorly ex-
tended, sub-elliptical. Shell thin. Sculpture
finely decussate. Periostracum pilose, per-
sistent. Hinge weak, teeth in two series on a
low arch, ligament Type D. Adductor scars
large, sub-equal, with very fine buttress lines.
Internally striate. Margin smooth. Foot large,
toe and heel not elongate, pedal retractors
simple, posterior pair large. Byssus gland
present but very small, no byssus observed.
Gill axis orientated vertically with very little
musculature. Mantle edge thickened, especi-
ally postero-ventrally (App. Figs. 6C, 24, and
Zn):

Habitat: Muds, muddy sand and muddy
gravel mixtures.

Bathymetric range: 80-500 m.

Distribution: Antarctic Ocean.

Species complement: Limopsis lilliei Smith,
1885; L. hirtella Mabille & Rochebrune, 1889;
L. enderbyensis Powell, 1958 and L. scotiana
Dell, 1964.

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MALACOLOGIA, 1981, 21(1-2): 95-110

ASPECTS OF THE ADAPTIVE MORPHOLOGY OF MESODESMA MACTROIDES

(BIVALVIA: MESODESMATIDAE)

Walter Narchi

Departamento de Zoologia, Universidade de Sao Paulo, Caixa Postal 20.520, 01000
Sao Paulo, Brasil

ABSTRACT

Mesodesma mactroides Deshayes, 1854 lives in southern Brazil, occurring in shallow water
on clean sand beaches where there is much wave action. M. mactroides is infaunal and pos-
sesses a number of morphological adaptations that suit it for a life in sandy beaches and for
feeding in water with suspended particles. The most significant of these adaptations concern the
organs of the mantle cavity. A comparison is made between M. mactroides and other infaunal
mesodesmatids.

Interest in this species also centres around its habit of living infaunally, possessing a well-
developed foot, an elevator pedal muscle and a wedge-shaped shell well designed for high
speed burrowing, particularly by young animals. Adult clams are found 15-20 cm deep. They
have a thin shell and two well developed and separate siphons. Siphonal hearts in M.
mactroides are described for the first time; they are rounded structures located between the
internal openings of the exhalant and inhalant siphons and contract spontaneously or under
slight stimulation. The principal function of the siphonal hearts seems to be the pumping of blood
into the long siphons, which possibly act as respiratory organs similar to the mantle and gills, or
the long siphons may require an accessory pump in order to circulate blood within them. No
other bivalves with long siphons are known to have similar structures. The major structural
features and ciliary currents of M. mactroides are described; its functional morphology is similar

to that of related genera such as Mactra, Spisula, Lutraria and Caecella.

INTRODUCTION

The wide post-Paleozoic radiation of in-
faunal bivalves led to a preponderance of new
Mesozoic and Cenozoic groups which were
burrowers feeding by means of siphons
(Stanley, 1968). Infaunal bivalves are thus of
primary importance in most of the benthic
communities of modern seas _ (Thorson,
1957). The bivalves which burrow in soft sub-
strata may be active or more or less seden-
tary, and often live well below the sediment-
water interface. According to Stanley (1968),
life habit data suggest that bivalve adaptive
radiation is related to mantle fusion and the
development of siphons. There is a general
agreement among bivalve taxonomists that
most of the commonly recognized bivalve
superfamilies, essentially similar to the
“Stirps” of Thiele (1934), represent natural
groups of related taxa.

The superfamily Mactracea appeared in the
late Mesozoic (Cretaceous) and existed
throughout the Cenozoic. As with most
heterodont bivalve superfamilies, the

Mactracea are restricted to suspension-feed-
ing with eulamellibranch ctenidia.

The paleontological records show that the
mesodesmatid ancestral stock originated in
Australasia, whence it gradually invaded
South Africa, New Zealand, the Antarctic and,
in successive migrations, South America.
From the Tertiary deposits of Patagonia there
are no fossil records. Ihering (1907) believed
that Mesodesma appeared in South America
in the late Pliocene or possibly in the early
Pleistocene during a great migration of mol-
luscs from the Antarctic, following two cold
currents: the Malvinas on the east coast and
the Humboldt on the west coast. This migra-
tion was probably caused by decreasing tem-
peratures towards the end of the Tertiary and
early Quaternary periods. According to Iher-
ing, the dispersion of Mesodesma on the
Patagonian coast occurred during the
Pleistocene and has only recently encom-
passed the Brazilian littoral, delayed by a
zoogeographic barrier, the mouth of La Plata
River.

Recent studies on the genus Mesodesma

(95)

96 МААСН!

are mainly concerned with taxonomy, shell
morphology, anatomy and ecology (lhering,
1897; Lamy, 1914; Carcelles, 1939; Castel-
lanos, 1948; Coscaron, 1959; Davis, 1964,
1965, 1967; Stanley, 1970; Olivier et al., 1971;
Beu, 1972; Habe, 1973). Purchon (1960) has
described the stomach of Atactodea, re-
garded by Thiele (1934) as a section of the
genus Mesodesma, and Allen (1975) de-
scribed the functional anatomy of Meso-
desma arctatum, restricted to the northwest
Atlantic.

Except for the thin shells which are not dis-
proportionately heavy as Allen (1975) de-
scribed for Mesodesma arctatum, М.
mactroides Deshayes, 1854 agrees with the
general characters of the family Mesodes-
matidae cited by Cox et al. (1969). The only
difference is that the hinge of the specimens
found in Sao Paulo is not strong and the teeth
are very poorly developed.

Mesodesma mactroides occurs from the
southern part of Brazil to Patagonia (Carcel-
les, 1944). It is a moderately frequent shallow
water species and is common in Brazilian
waters where it has been recorded along the
coasts of Rio de Janeiro (Rios, 1970, 1975),
Sao Paulo (Lange de Morretes, 1949) and
Parana (Gofferje, 1950). It was first recorded
from Brazilian waters by Ihering (1897) and is
called “sernambi,” “marisco” or “marisco
branco” by the local fishermen. The animals
are eaten by the coastal population steamed
or with rice, and it is an important food supply
mainly in Rio Grande do Sul, Uruguay and
Argentina. Deshayes (1854) described M.
mactroides without giving a type-locality.
Carcelles (1939) gives a good systematic ac-
count of the species. Ihering (1897) refers to
М. arechavalettoi known as “almeja amarilla”
from the mouth of La Plata River, which 15
bigger, robust and with a yellow periostracum.
Lamy (1914) and Carcelles (1939) consid-
ered М. arechavalettoi to be М. mactroides.
The animals from Sao Paulo have a trans-
parent periostracum, and a much thinner shell
than the specimens from Argentina.

Isolated references to Mesodesma mac-
troides are found mainly in systematic ac-
counts; Castellanos (1948) studied its anat-
omy and Olivier et al. (1971) described the
life-history, ecology and observed a popula-
tion of M. mactroides during a period of two
years at Mar Azul, a resort 115 km N of the
city of Mar del Plata, Argentina. Until now, no
studies of the functional morphology of M.
mactroides have been undertaken.

MATERIALS AND METHODS

Living specimens were obtained from
beaches at Santos and Bertioga on the coast
of Sao Paulo, Brazil. They were collected dur-
ing low tide from clean sand in disturbed wa-
ters with wave movement. The water con-
tained a large amount of suspended material.
The species is a rapid burrower; the pointed
foot emerges from the elongate antero-ventral
region of the shell and probes the sand quick-
ly to gain a foothold. Erection of the shell is
normally accomplished by a single burrowing
sequence which pulls the animal directly
downward without the rocking movement
described for Mesodesma arctatum by
Stanley (1970).

Small specimens of Mesodesma mac-
troides measuring less than 2cm long co-
occur with Donax hanleyanus at the Santos
beaches, in the lower eulittoral. M. mac-
troides is flushed from the sand by the ad-
vancing surf and transported up the beach.
The clams would be carried down in the
backwash, but by extending their siphons and
foot to act as brakes, they prevent being
washed away.

Adult Mesodesma mactroides clams, un-
like M. arctatum (Allen, 1975), are found 15-
20 ст deep (Fig. 1) in firm sand, with the
large foot extended as an anchor, their long
siphons lying flush with the surface of the
sand. M. mactroides lives buried at depths
about four times greater than that of M.
arctatum (Stanley, 1970), i.e. about twice the
length of the shell of the latter. The beaches of
Sao Paulo, where the animals were found,
are flat, and when the tide recedes, the bi-
valves are stranded above the water line. The
sand becomes more compact during the ebb
tide. The mean particle diameter is less than
0.5 mm.

The clams could usually be found by locat-
ing the small siphon holes on the surface of
the sand. Only adult clams, in their deep bur-
row, can hold their position on the beach
using their enlarged foot. Because the smaller
clams are anchored less firmly, they are
flushed out more frequently and washed far-
ther up the beach than the large clams.

The animals were collected during low tide
by digging into the sand with a small mattock.

| will describe the structure, ciliary currents
of feeding and digestion and other functional
adaptations of Mesodesma mactroides in re-
lation to their environment. Drawings are of
relaxed and preserved specimens. Magnesi-

MESODESMA MORPHOLOGY 97

wog

FIG. 1. Mesodesma mactroides. External view of
the left side. Living specimen digging in firm sand
with its large foot extended.

um sulphate was used as a relaxing agent,
ciliary currents were studied using carborun-
dum, carmine and Aquadag suspensions.
Sections (6 to 8 um thick) were made of tis-
sues fixed in Bouin’s fluid, stained with
Ehrlich’s haematoxylin and eosin, and Mal-
lory’s Triple Stain.

Living specimens were observed at the De-
partamento de Zoologia, Universidade de
Sao Paulo.

FUNCTIONAL MORPHOLOGY
The shell

Contrary to the other species of Meso-
desma, M. mactroides does not have a ro-

bust shell. It is thin, a little inflated, elongate-
oval, inequilateral, tapering slightly toward the
rear, rostrate behind, the rostration prolonged
to a moderately acute tip. The anterior margin
is acute, the ventral margin almost straight,
the posterior margin rounded below and ob-
liquely subtruncate above. Beaks low, situ-
ated at the posterior third. The shell surface is
slightly marked by delicate concentric lines,
covered by a transparent periostracum.

The anterior muscle scar is relatively long
and lenticular, with a ragged inner and a
smooth outer margin; the posterior scar is
broadly oval. The pallial sinus is asymmet-
rically arcuate. It rises from the inner and
lower surface of the posterior adductor scar,
is obtusely subangular at the forward end,
and joins the faint pallial line near the poste-
rior third.

The hinge plate (Fig. 2) is not strong and
broad as in Mesodesma arctatum (Allen,
1975). There are two lateral teeth and two
cardinal teeth with an accessory lamina in the
left valve. In the right valve there are two
cardinal and three lateral teeth, which are
smooth without serration as in M. arctatum
(Allen, 1975).

The external ligament is not prominent but
a subtriangular chondrophore is well devel-
Oped in both valves.

The lunule is rudimentary and the escutch-
eon vestigial. The surface of the shell is
marked by delicate concentric growth lines.
The shell is generally white but in some speci-
mens the shell margin is darkly colored.

The periostracum is translucent but in a few
specimens it is yellowish.

The shell of the largest animal studied
measured 5.8 cm in length, 3.2 cm in height,
and 1.6 cm in width.

The siphons

The siphons are separate and well devel-
oped. In a specimen 5 cm long, the siphons
were both almost 15 ст long. The detailed
structure is shown in Fig. 3. The external sur-
face of both siphons bears two longitudinal
rows of small, colourless, sensitive papillae
without surrounding pigmentation, as found in
Ensis ensis (Deshayes, cited in Haas, 1934).
Franc (1960) described two rows of small
papillae on the exhalant siphon and only one
on the inhalant siphon of Ensis ensis (not
Corbula mediterranea as he states: compare
fig. 312 of Haas, 1934, with fig. 1633 of Franc,

98 МААСН!

FIG. 2. Mesodesma mactroides. Internal view of the hinge plate. a, right valve; b, left valve.

1960). The inhalant aperture is fringed with
three cycles of tentacles surrounding the aper-
ture, and is similar to that of Mesodesma
cornea (Fischer, 1887). The innermost series,
the largest and the most ramified, is formed
by eight tentacles. They are directed inwards
when the animal is pumping water. These
tentacles are interspersed by small accessory
papillae. The two series of smaller foliose
tentacles surround the inner. They too are
directed inwards so that the inhalant aperture
is, in effect, covered by a coarse sieve. The
48 tentacles are unpigmented, unlike those of
Tivela mactroides (Narchi, 1972). The aper-
ture of the exhalant siphon is a little smaller
than that of the inhalant. Twenty simple tenta-
cles surround the exhalant opening as in 7.
mactroides (Narchi, 1972). In specimens
2 cm in length, six tentacles sometimes are
better developed and have a divided tip. An
extensive siphonal flap is developed across
the inner opening of the inhalant siphon. This
is a vertical extension of the posterior margin
of the septum dividing inhalant from exhalant
channels.

The positions of the siphons in life are
shown in Fig. 1.

FIG. 3. Mesodesma mactroides. The siphons of
the live animal. The arrows show the direction of
the inhalant and exhalant currents.

MESODESMA MORPHOLOGY 99

The circulatory system and the
the siphonal hearts

Some invertebrates possess certain periph-
eral blood vessels specialized to pump blood
into organs that would otherwise have little
circulation. Among molluscs the best known
are the “gill hearts” of cephalopods and the
“accessory hearts” in oysters (Hopkins
1934a, 1934b, 1936).

Removal of one mantle lobe of M. mac-
troides exposes a pair of well-defined, round-
ed structures within the supra-axial chamber
just below the inner opening to the exhalant
siphon (Fig. 4). These structures, recorded
here for the first time in the Bivalvia, contract
spontaneously or under mechanical stimula-
tion. They are not the peripheral blood ves-
sels that Galtsoff (1964) observed in Cras-
sostrea virginica, and | term them siphonal
hearts.

The well-developed muscular fibres of the
walls of the siphonal hearts resemble those of
the ventricle (Fig. 5).

The connection of the siphonal hearts to
other blood vessels has been studied using
the modified injection method of Galtsoff

(1964). When the ventricle is injected, fluid
enters the anterior and posterior aortas. From
the posterior aorta the fluid passes to the
aortic bulbs and from here it enters the si-
phonal hearts. Injecting the siphonal hearts
fills the arteries of the siphons.

The mantle and its ciliary currents

The two mantle lobes are unfused anterior-
ly, forming a large pedal gape. The two man-
tle lobes fuse mid-ventrally, this fusion ex-
tending up to the inhalant siphonal aperture.
Fusions also occur between inhalant and ex-
halant siphons and dorsal to the exhalant si-
phon. Only the inner folds are fused. The
middle mantle fold is moderately well devel-
oped and bears two regular rows of small
papillae, those external with two or four digi-
tate projections.

The inner surface of the mantle is ciliated
and its ciliary currents are shown in Fig. 6. On
each lobe they converge mid-ventrally, poste-
rior to the foot, and enter a ventral tract
formed by erectile mantle folds that may be
elevated and bent toward each other until
they almost or quite meet, forming the “waste

0,5 mm

FIG. 4. Mesodesma mactroides. A transverse section through the siphonal hearts showing the arrangement

of muscle fibres.

100 МААСН!

en SS SSS =
о NE | N

N N Q 4
> . ANS S SS
x ; OS : x à N :
SOR NN SI
ARE ECA SSS

FIG. 6. Mesodesma mactroides. The inner surface of the right mantle lobe to show the ciliary cleansing
currents.

MESODESMA MORPHOLOGY 101

canal’ (Kellogg, 1915). The accumulated
waste from the visceral mass and palps usu-
ally passes into this canal, in which all parti-
cles are carried backwards as recorded for
Spisula, Lutraria (Yonge, 1948), Mesodesma
arctatum (Allen, 1975), and Caecella
chinensis (Narchi, 1980). On the mantle sur-
face of M. mactroides, the direction of the
ciliary currents is different from that of M.
arctatum (Allen, 1975) and Mactra solidissi-
ma (Kellogg, 1915), and is very similar to that
of Lutraria lutraria and С. chinensis. On the
posterior two-thirds, particles are carried for-
wards, and from there, ventrally directed cur-
rents convey them to the entrance of the
waste canal. Currents around the margin of
the pedal gape carry material inwards to the
same point. The fusion of the mantle edges
makes ventral ejection of waste material im-
possible, this taking place via the inhalant
siphon. As in M. arctatum (Allen, 1975) and
M. solidissima (Kellogg, 1915), a well-devel-
oped siphonal membrane rejects large parti-
cles downward, and acts, like the waste
canal, in preventing undesirable material from
being carried back into the mantle chamber.
As in M. arctatum, M. mactroides does not
possess a fourth pallial aperture. :

Musculature, foot and pedal gape
The adductor muscles lie ventral to the

hinge line and differ considerably (Fig. 7). The
anterior adductor (aam) is a relatively long,

—

narrow and elongate muscle, slightly tapering
at the posterior end, transverse and curved
upward. Its posterior surface is indented by a
deep groove. Into the posterior region of the
groove pass a few fibres of the protractor
pedal muscle (pa). The anterior adductor
muscle lies in front of the mouth and has a
different form from that of Mesodesma
arctatum (Allen, 1975). The posterior adduc-
tor (pam) is oval in section. The disposition of
the muscles is similar to that of Donax vittatus
(Graham, 1934) and D. hanleyanus (Narchi,
1978).

The foot (f) is axe-shaped without a flat-
tened sole. There is no byssus gland.

The outermost muscular layer of the foot
comprises the protractor muscles (pa). These
pass to the anterior adductor and are inserted
either on the ventral surface of that muscle or
on the parts bordering the transverse groove.

The anterior pedal retractor (arm) com-
prises two layers separated by a component
of the posterior pedal retractor muscle. One
layer of the former muscle intermingles with
the layers of the pedal protractor and com-
prises a thin sheet of more or less circular
fibres. The second layer of the anterior pedal
retractor lies deeper in the foot.

The posterior pedal retractor (prm) is also
divided into two in the ventral region of the
foot.

The two pedal elevator muscles (e) form
the innermost pedal muscles. Like the poste-
rior retractor muscles, they fuse in the foot

PEN prm

BAP SZ

EEE }

FIG. 7. Mesodesma mactroides. The arrangement of the musculature; aam, anterior adductor muscle; arm,
anterior retractor muscle; e, elevator pedal muscle; f, foot; pa, protractor pedal muscle; pam, posterior

adductor muscle; prm, posterior retractor muscle.

102 МААСН!

only to separate subsequently. п Caecella
chinensis (Narchi, 1980) these muscles are
poorly developed, but in Donax hanleyanus
(Narchi, 1978) and D. vittatus (Yonge, 1949)
they are well developed. Castellanos (1948)
did not recognize the elevator muscles in the
specimens of M. mactroides she studied. The
mantle edge is fused to form the inhalant and
exhalant siphons. Fusion ventral to the in-
halant siphon extends for about half the
length of the ventral margin of the mantle,
thus limiting the pedal gape.

The ctenidia

The arrangement of organs in the mantle
cavity after removal of the left valve and man-
tle lobe is shown in Fig. 8. The siphons, foot
and posterior mantle lobe are somewhat con-
tracted.

The form of the ctenidia and the general

course of the ciliary currents are shown dia-
grammatically in Fig. 9. The inner demibranch
(id) is somewhat longer than the outer (od).
Gill ciliation is of Type C (la) (Atkins, 1937),
due to the presence of two oralward currents:
one in the ventral food groove of the inner
demibranch, the other in the ventral, un-
grooved, margin of the outer demibranch.
Allen (1975) described particles in Meso-
desma arctatum moving anteriorly along the
margin of the outer demibranchs being trans-
ferred to the inner demibranchs. The ctenidia
of M. mactroides are similar to those of
Donax hanleyanus (Narchi, 1978) and
Caecella chinensis (Narchi, 1980) in the pos-
session of an incipient oralward current in the
posterior region of the ventral margin of the
outer demibranch only.

On the ascending and descending lamellae
of both demibranchs, there are downward
ciliary currents on the crests of all filaments

dd u

2 cm

FIG. 8. Mesodesma mactroides. The organs of the mantle cavity viewed from the left side after removal of
the left shell valve and mantle lobe; aam, anterior adductor muscle; arm, anterior retractor muscle; dd,
digestive diverticula; e, elevator pedal muscle; ex, exhalant siphon; f, foot, id, inner demibranch; Ир, inner
labial palp; in, inhalant siphon; od, outer demibranch; olp, outer labial palp; p, periostracum; pa, protractor
pedal muscle; pam, posterior adductor muscle; pg, pedal gape; prm, posterior retractor muscle; sae, supra-
axial extension of outer demibranch; sh, siphonal heart; u, umbo; wc, waste canal.

MESODESMA MORPHOLOGY 103

and in the plical troughs. In the proximal re-
gion of the ctenidial axis is an additional oral-
ward current fed by upwardly beating cilia on
both descending lamellae. On each side of
the body, there are thus three oralward cur-
rents as in Tivela mactroides (Narchi, 1972).
A supra-axial extension (sae) of the outer
demibranch is also present.

Mesodesma mactroides has moderately
plicate lamellae as in Donax hanleyanus. The
plicae are shallow and occur over the greater
part of both lamellae with an average number

FIG. 9. Mesodesma mactroides. Diagrammatic
vertical section through one half of the body to
show the ciliary currents of the ctenidium and man-
tle; id, inner demibranch; m, mantle lobe; od, outer
demibranch; pe, pericardium; re, rectum; sae,
supra-axial extension of outer demibranch; sc,
supra-branchial chamber; wc, waste canal.

of 12 filaments per plica, ranging from a mini-
mum of ten to a maximum of fifteen in the
outer and inner demibranchs. Ridewood
(1903) observed fewer т М. novae-
zelandiae. Also as in this species and species
of Donax, M. mactroides has no differentiated
principal filaments. Pelseneer (1911) showed
that M. complanata has unplicate lamellae,
while М. mactroides has slightly plicate
ctenidia. Pelseneer (1911) found in Donax
species with either flat, slightly plicate, or
strongly plicate lamellae. Narchi (1978) found
the ctenidium of Donax hanleyanus to be
variably plicate.

The filaments (Fig. 10) are separated by
laterofrontal cilia (№), 5 um long. The frontal
cilia (fc), 4 ит in length give way to longer
terminal cilia in the distal region and which are
28 ит in length.

The ventral tips of the anterior filaments of
the inner demibranch only are inserted and
fused to a distal oral groove (Fig. 11A) and the
ctenidial-labial palp junction is thus of Cate-
gory И (Stasek, 1963).

The labial palps
The palps are triangular and relatively long.
The inner faces are deeply plicate and the

outer faces smooth (Fig. 11A). The dorsal
margin of each palp is relatively wide and

lfc

Ici

20 Um

FIG. 10. Mesodesma mactroides. A transverse
section of two filaments of the inner demibranch
showing the arrangement of the various ciliary
groups; fc, frontal cilia; Ici, lateral cilia; lfc, latero-
frontal cilia.

104 МААСН!

FIG. 11. Mesodesma mactroides. A, The relationship between inner demibranch and labial palps showing
ciliary currents and acceptance tracts; B, diagrammatic representation of the ciliary currents of two folds of
the inner surface of the labial palp. (For explanation see text.)

smooth. The narrow ventral margin carries
particles backwards to the tip, whence they
are passed into the mantle cavity. Particles
collected on the outer faces of the palps are
carried over onto the dorsal margin of the inner
faces. Particles carried along the dorsal mar-
gin are usually caught up by cilia on the inner
palp surface and carried forwards.

Small particles that have passed along the
ventral marginal food grooves of the ctenidia
tend to pass directly into the groove between
the palps. Larger particles travelling along the
ventral marginal food groove usually drop
onto the visceral mass or mantle before
reaching the palps.

Particles arriving at the palps from the
ctenidial axis usually pass into the distal oral
groove and then into the groove between the
palps. In addition, the palps have sorting cur-
rents on their inner faces. In Fig. 11B, the
following symbols are used to differentiate the
ciliary tracts of adjacent palp folds: a) an ac-
ceptance tract which passes small particles
oralward over the crests of the folds; c) a re-
jection tract passing large particles into the
troughs, from which d) removes unwanted
particles; b) and e) are currents which sort
particles of intermediate size to be selected or

rejected. The latter particles are either re-
jected via the dorsal or ventral edges of the
palps or reach the proximal oral groove. The
ciliary tracts of the palps in Mesodesma
mactroides are similar to those of Asaphis
dichotoma (Narchi, 1980).

The alimentary canal

The mouth (Fig. 12) opens into a fairly long
oesophagus which enters the antero-dorsal
part of the stomach. As in Mesodesma
arctatum (Allen, 1975) the oesophagus is
ciliated with narrow longitudinal ridges along
its entire length. According to Castellanos
(1948), the oesophagus of M. mactroides is
short. There is no appendix in the postero-
dorsal region of the stomach.

Mesodesma mactroides is similar to spe-
cies of the Mactridae in possessing a sepa-
rate style sac and mid-gut.

The mid-gut and style sac are similar to
those of Donax hanleyanus (Narchi, 1978)
and Caecella chinensis (Narchi, 1980). Both
open near to each other on the anteroventral
wall of the stomach. The long and curved
style sac extends antero-ventrally from the
stomach to a point level with and anterior to

MESODESMA MORPHOLOGY 105

2 cm
(|

FIG. 12. Mesodesma mactroides. А diagram of the dissected alimentary canal, as seen from the left side.

the mouth. The mid-gut leaves the ventral
right wall of the stomach. It passes forwards
and curves ventrally into the foot. Unlike D.
vittatus (Graham, 1934), it does not coil.
Castellanos (1948) described two coils in the
intestine of M. mactroides, but these were
not observed in my specimens. On reaching
the point where the style-sac bends anteriorly,
the mid-gut passes to the left posterior side of
the style sac and then ascends to the heart. It
enters the pericardial cavity on its anterior
wall again without coiling. The hind-gut
passes through the pericardial cavity and the
ventricle and opens via the anus on the poste-
rior face of the posterior adductor muscle.

The stomach

In a series of studies on the structure of the
bivalve stomach, Purchon (1960) recognized
five types. Mesodesma mactroides has a
stomach of type V and is typical of the
Mesodesmatidae.

The large and irregular stomach (Fig. 13) is
similar to that of Atactodea glabrata Lamarck
(Purchon, 1960). The slender oesophagus
(0), Opens into the anterior face of the stom-
ach. There is a large globular swelling at the
left anterior border of the opening of the style-
sac (ss) into the stomach, and this swelling
extends forward as a ridge, which runs ante-
riorly over the floor of the stomach.

As in Atactodea glabrata (Purchon, 1960),

Mesodesma mactroides does not possess a
minor typhlosole.

The greatly swollen major typhlosole (ty) is
accompanied throughout its course by the
intestinal groove; it passes forwards and onto
the right side of the stomach, entering a broad
and shallow right caecum (rc) within which it
forms a half circle before emerging. Eight
ducts from the digestive diverticula opens into
the right caecum.

From the right caecum the typhlosole ex-
tends transversely across the anterior wall of
the stomach to enter the extensive left
caecum (Ic) which receives fourteen ducts
from the digestive diverticula. The major
typhlosole forms a loose spiral of about two
and a half turns on the median and posterior
walls and terminates on its posterior wall near
the opening.

The dorsal hood (dh) is relatively small and
lies on the postero-lateral wall of the stom-
ach. On its anterior wall there is an extensive
sorting area (Sag) of ridges and grooves,
which extends over the roof of the stomach to
the right side of the oesophageal opening.
Cilia beat downward in the grooves while an
acceptance tract passes from right to left,
along its anterior border conveying particles
into the dorsal hood. This tract is delimited
anteriorly by a ridge which passes from the
left border of the oesophagus to the opening
of the dorsal hood. The oesophageal aperture
has a series of papillae (pr) which lie on its

106 МААСН!

FIG. 13. Mesodesma mactroides. A, the interior о the stomach seen after being opened by an incision along
the right wall, B, right caecum; C, left caecum; dh, dorsal hood; gs, gastric shield; Ic, left caecum; Ip, left
pouch; mg, mid-gut; 0, oesophagus; pr, processes ornamenting the oesophageal orifice; r, ridge; rc, right
caecum; заз, principal sorting area of the dorsal hood; sas, sorting area on the posterior wall of the dorsal
hood; sag, sorting area of the left pouch; sag sorting area on the anterior roof of the stomach; ss, style sac; ty,

major typhlosole.

right side and ventrally between it and the in-
testinal groove. Small papillae occur on the
right side of the sorting area (Sag) and gradu-
ally increase in size and complexity along a
series of about twenty such papillae. Each
one bears a double series of lobes on its up-
per border. A similar series of papillae has
been found in Pholadidea loscombiana
(Purchon, 1955), Mactra mera, Caecella
cumingiana (Purchon, 1960) and С. chinen-
sis (Narchi, 1980).

Dorsalward, ciliary currents occur on the
smooth posterior sides of these papillae and,
along the anterior side of the bases of the
papillae, a ciliary current passes from left to

the right. These papillae exhibit considerable
muscular activity.

On the roof of the dorsal hood there is a
sorting area (Sa3). Cilia on this convey parti-
cles over the crests of the folds towards the
apex of the dorsal hood. In the grooves be-
tween the folds cilia beat forward into a rejec-
tion tract. The sorting area extends to the right
side of the stomach. The rejection tract which
discharges material into the intestinal groove
is separated from the posterior border of the
right caecum by a well-defined ridge (r). On
the posterior wall of the dorsal hood there is a
sorting area (Sas) of relatively large folds, on
which cilia beat ventrally and out of the dorsal

MESODESMA MORPHOLOGY 107

hood where the area joins a longitudinal
ridge. As in Mactra mera, this sorting area
terminates on the right side of the stomach
where there is a conspicuous, ventrally pro-
jecting swelling which normally arches over
the intestinal groove to touch the major
typhlosole.

The left pouch (Ip) lies on the left anterior
wall of the stomach, between the left caecum
and the dorsal hood. There is no special line
of demarcation between these apertures.
Four digestive ducts enter the left pouch in
Mesodesma mactroides; Atactodea glabrata
(Purchon, 1960) has eight ducts. A narrow
band of fine transverse ridges and grooves
(Sag) is present on the floor of the left pouch,
penetrates the apex and then passes on its
dorsal side.

About eight ducts from the digestive diver-
ticula open along the posterior border of a
sorting area on the roof of the stomach (sag).

The gastric shield is firm and sends a deep
flare into the mouth of the dorsal hood; it also
envelops the posterior border of the left
pouch.

| did not observe a small sorting area of fine
radiating ridges and grooves on the posterior
border of the aperture of the mid-gut that is
present in Atactodea glabrata (Purchon,
1960).

DISCUSSION

Mesodesma mactroides is ап intertidal
suspension feeder, well adapted to its mode
of life. The siphons are similar to those spe-
cies of similar habits (Tivela mactroides:
Narchi, 1972), having numerous branched
tentacles, which curve over the aperture to
form a grate when the animal is pumping
water.

Mesodesma mactroides lives on open
sandy beaches, where large numbers of par-
ticles are constantly lifted into suspension by
wave movement.

Mesodesma mactroides occurs in a firm
substratum and has a well-developed foot, an
elevator pedal muscle and a wedge-shaped
shell, well designed for high speed burrowing,
particularly in young animals. Small speci-
mens (with Donax hanleyanus) in the Santos
beaches were flushed from the sand by the
advancing surf and carried up the beach in
the uprush. Instead of being carried down with
the backwash they extended the foot to act as
a braking device.

The clams are highly specific with regard to
their choice of sand and are absent from
some beaches of our littoral. Few other ani-
mals can survive in the places that have the
right requirements. As a result, populations of
Mesodesma mactroides develop without
much competition. The same type of habitat is
shared only with Donax hanleyanus. The
populations of these two species compete
when M. mactroides is of small size. Thus, in
places where adult M. mactroides occur, it is
usually the most abundant in terms of bio-
mass and may be regarded as dominant in its
habitat. M. mactroides is a good indicator of
beach type and condition.

The ctenidia of Mesodesma mactroides
are of type C (la) (Atkins, 1937), the same
type as in Donax hanleyanus (Narchi, 1978).
This similarity probably results from con-
vergent adaptation to the same habitat.

As stated by Allen (1975) for Mesodesma
arctatum, “the cilia of the posterior half of the
mantle, dorsal to the mantle fold, direct parti-
cles ventrally and anteriorly where they either
join the main current from the palp to the fold
or are directed onto the dorsal surface of the
fold. At the dorsal junction of the fold and gen-
eral mantle surface there is an anteriorly di-
rected ciliated tract to the anterior end of the
fold.” In M. mactroides, all currents from the
posterior half of the mantle convey particles
anteriorly where they join the main currents
from the palp, entering the rejection canal be-
tween the fold and inner muscular lobe. This
difference probably is related to the great de-
velopment of the pallial sinus in M. mac-
troides.

Mesodesma mactroides possesses a
waste canal, in which pseudofaeces can ac-
cumulate without interfering with the inflow of
water through the inhalant canal. The waste
canal is roofed by the mantle folds which ter-
minate posterior to the siphonal membrane in
the same manner as in M. arctatum (Allen,
1975). Similar longitudinal folds are also
present in the Mactridae.

A siphonal membrane is present in Meso-
desma mactroides, in M. arctatum (Allen,
1975) and in the Mactridae (Yonge, 1948).
Yonge (1948) concluded that such a structure
evolved in shallow-burrowing animals as an
adaptation to life in silty waters.

Unlike Schizothaerus nuttalli, the mantle
edges of Mesodesma mactroides are not
fused as far forward as the anterior end of the
mantle folds. The mantle folds and the waste
canal end behind the siphonal membrane and

108 МААСН!

accumulated waste is ejected through the
long inhalant siphon in the usual manner.
Kellogg (1915) sugested that the function of
the siphonal membrane was to pass large
particles downwards onto the mantle edges,
and away from the gills, especially when
much sediment is present in the inflowing
water. Yonge (1948) concluded that the
membrane is an adaptation for life in silty
water and that for this reason Schizothaerus
has retained the siphonal membrane. M.
mactroides also has a siphonal membrane,
probably because wave action in its habitat
lifts up large amounts of sediment.

Siphonal hearts in Mesodesma mactroides
are described for the first time. They are
rounded structures located between the in-
ternal openings of the exhalant and inhalant
siphons and they contract spontaneously or
under slight stimulation. They differ from the
accessory hearts of Crassostrea virginica
(Galtsoff, 1964) and the pulsating vessels of
Ostrea gigas (Hopkins, 1934a, 1934b, 1936).
The principal function of the siphonal hearts
seems to be the pumping of blood into the
long siphons, which possibly act as respira-
tory organs similar to the mantle and gills or
the long siphons may require an accessory
pump in order to circulate blood within them.
Counts of the rates of pulsation of the heart
and siphonal hearts show that they act inde-
pendently. The rate of pulsation, as in the ac-
cessory hearts of oysters, is probably deter-
mined by the rate at which they fill with blood,
and is thus regulated by the heart. No other
bivalves with long siphons have similar struc-
tures.

The alimentary canal of Mesodesma
mactroides is similar to that of Donax vittatus
(Graham, 1934) but with some differences:
the intestine of adult M. mactroides is not
coiled and the style sac is smaller.

The mid-gut and style sac of Mesodesma
mactroides are separated. The stomach has
much the same structure and functions as
that of a typical suspension-feeding eulamel-
libranch. It is essentially similar to other
mesodesmatids studied earlier. The oesoph-
ageal orifice possesses a series of pinnate
lobes on the ventral and right borders. A simi-
lar series of papillae have been recorded
for Pholadidea loscombiana (Purchon,
1955), Mactra mera, Caecella cumingiana
(Purchon, 1960), Mesodesma arctatum
(Allen, 1975) and Caecella chinensis (Narchi,
1980). These lobes are muscular and pos-

sibly prevent large particles entering the
stomach.

SUMMARY

Mesodesma mactroides Deshayes, 1854
is an inhabitant of clean sand in waters dis-
turbed by wave movement. The species oc-
curs from southern Brazil to Patagonia. It lives
infaunally and possesses many features
adapting it for life in sandy beaches: (1) lack
of a robust shell; (2) anterior muscle scar long
and lenticular, posterior one broadly oval; (3)
long separate siphons; (4) a pair of rounded
structures in the supra-axial chamber just be-
low the inner opening to the exhalant siphon,
recorded here for the first time and called
siphonal hearts; (5) moderately plicate lamel-
lae without differentiated principal filaments;
(6) waste canal conveying particles and ac-
cumulated waste from the visceral mass and
palps backwards; (7) no appendix in the
postero-dorsal region of the stomach; (8)
separate style sac and mid-gut; (9) many
Openings from stomach into digestive diver-
ticula.

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MALACOLOGIA, 1981, 21(1-2): 111-148

EVOLUTION AND ADAPTIVE RADIATION ОЕ WOOD-BORING
BIVALVES (PHOLADACEA)

K. Elaine Hoagland! and Ruth D. Turner2

ABSTRACT

Wood-boring bivalves represent a major worldwide adaptive radiation in the marine environ-
ment. This paper reviews that radiation and the morphological adaptations central to it. The fossil
record, population genetics, and some ecological features of some Teredinidae are discussed
as they bear upon the adaptive radiation. The wood-borer radiation began with the evolution of
woody plants, which provide substrate in the form of driftwood and salt-tolerant living plants. Key
adaptations were, first, the ability to bore into wood, and second, the ability to use wood for food.
There were actually radiations in two related families of the superfamily Pholadacea: the
Pholadidae (27 fossil and living genera, 5 of which are wood-borers) and the Teredinidae (15
living genera, all obligate wood-borers).

The Pholadidae and the Teredinidae share some anatomical features such as the reduced
hinge, projections inside the shell, large pedal gape, and discoid foot, although these may be
convergent. The relative success of the teredinid wood-borer radiation, compared with the
pholads, is probably due to the development of a calcareous tube and attachment of the siphonal
retractor muscles to it, elongation of the body, reduction of the shell, and the evolution of pallets
to close the tube. The pholads have not undergone shell reduction and they lack pallets. They do
have accessory plates on the shell.

The wood-borer radiation, based on a patchy and temporary substrate, has led to variable-
sized, paichily-distributed, inbred populations of most species. This population structure pro-
vides mechanisms for both the complex speciation pattern and the wide ranges of single species
that characterize the Pholadacea.

Features such as pallet shape are variable among teredinid species, illustrating multiple
solutions to acommon problem. Other features such as siphon morphology have clear functional
significance and hence can be assigned a role in the adaptive radiation of the Pholadacea.
Finally, there are examples of multiple selective pressures dictating the structure of one organ,
such as the adaptation of the gill for brooding young as well as for respiration and feeding.

Most Teredinidae are protandrous, but a few can function as simultaneous hermaphrodites,
and one has separate sexes with dwarf males. These modes of sexuality are related to life in
temporary habitats. Ways of coping with crowding are plasticity in size at maturity and cessation
of wood-boring in favor of filter feeding. Broad physiological tolerances help to insure dispersal to
new sources of wood and survival in estuaries. Species with planktonic development are not
more broadly distributed worldwide than those that brood the young and disperse as adults in
driftwood or boats.

Population genetical data involving 32 enzyme loci show striking species differences related to
dispersal. Bankia gouldi and B. fimbriatula with planktonic larvae are more diverse genetically
than two species with brooded larvae. A species with partial brooded development is intermedi-
ate.

The constraints of life in wood have made wood-borers unrivalled as opportunistic species,
hence the success of many species when introduced to new localities. A review of life histories
shows that teredinids have characteristics of both r- and K-selected species. The most important
traits are short generation time, a high rate of increase, and tolerance of crowding leading to
good competitive ability. Sympatric teredinids coexist because of the patchy temporal and
spatial availability of wood, allowing the presence of numerous species that reproduce at dif-
ferent times. One species can monopolize a piece of wood if availability of the wood and
competent teredinid pediveligers coincide. The spread of adult shipworms by man’s use of wood
in the marine environment could be responsible for slowing the speciation process by enhancing
the spread of species with genotypes adapted for colonization, and/or by increasing outbreeding
of all species.

Numerical taxonomic methods are applied to the character states of Pholadacean species in
order to develop hypotheses on the relationship of morphology to ecology and to develop

Lehigh University, Bethlehem, РА 18015, U.S.A.
2Museum of Comparative Zoology, Harvard University, Cambridge, MA 02138, U.S.A.

(111)

HOAGLAND AND TURNER

possible evolutionary sequences. А simple cladistic method using unique and unreversed char-
acters can elucidate relationships at the generic level. Both that method and phenetic analyses
reveal convergences of character states in the Pholadacea. Phenetic analyses emphasize simi-
larities among the taxa based оп wood-boring habits, while the analysis of unique characters
provides a possible sequence of taxa that developed from a rock-boring ancestor. Both methods
reveal problems in determining homologous characters.

Both numerical taxonomy and electrophoretic data support the current taxonomic structure of
the Pholadacea, except that the data suggest polyphyly of the Bankiinae. Also, the genus
Lyrodus may not be a natural, monophyletic group. Limited data available for Kuphus indicate
that its unique combination of primitive and specialized character states place it apart from the
other Teredinidae. In fact, the Kuphinae does not appear to be of equal taxonomic rank with the
Bankiinae and the Teredininae. Wood-boring may have evolved in two lineages of the Pholadi-
dae, one continuing into the teredinid lineage.

INTRODUCTION

Wood-boring bivalves are members of the
superfamily Pholadacea. They occur in ma-
rine, estuarine, and in a few places, virtually
freshwater (upper estuarine) environments.
Besides these bivalves, there are only a few
crustaceans (e.g., Sphaeroma and Limnoria)
capable of a marine wood-boring existence.
The adaptive radiation of the wood-boring bi-
valves, based as it is on the occupation of
wood is a narrow one, with severe limitations
on ecological deployment. Yet the wood-
borers include two related families in the
Pholadacea, 20 living genera, and approxi-
mately 175 living species found in all oceans.
The radiation can be interpreted as two paral-
lel radiations, perhaps in competition, repre-
sented by the two families.

We first review what is known of the evolu-
tion of those Pholadacea that are wood-
borers, based on the meager fossil record.
We then review the morphological features
characteristic of wood-boring clams in gen-
eral, and those characterisitc of the two major
families. We present new data on the popula-
tion genetics and ecology of six species, three
living sympatrically in Barnegat Bay, New
Jersey, and three living sympatrically in
southern Florida. We analyse some aspects
of the morphology, physiological tolerances,
population structure, life history character-
istics, zoogeography, and population genetics
of teredinids as they bear on the evolution of
wood-borers. The six species examined in
detail were chosen because they represent
several of the divergent patterns of life history
and ecology comprising the adaptive radiation
of the Pholadacea.

We analyse the characters of the Pholada-
cea using numerical taxonomic procedures, in
order to understand how the characters are
correlated, how they might be related to se-
lective pressures of the environment of wood-

borers, and how the taxa might be related (or,
at least, how similar they are). Finally, we
summarize the modes of evolution of the
wood-boring bivalves, with emphasis on limi-
tations to the adaptive radiation and on the
role of man in the present course of the radia-
tion.

METHODS
Morphology and Evolutionary History

The evolutionary history, functional mor-
phology, and zoogeographic data presented
here are based on the literature, especially
earlier works by one of us (Turner). The data
used to compile taxonomic characters for the
Pholadacea came primarily from Turner
(1954, 1955, 1956, 1962, 1965, 1966, 1971,
1972a & b, 1973), Purchon (1941), and
Knudsen (1961). Some details of shell shape
and umbonal reflection of the pholads were
omitted from the data matrix because it was
not possible to quantify them.

Population Dynamics

Data were obtained on the population
dynamics of teredinids from Barnegat Bay,
New Jersey, U.S.A. White-pine panels of
equal size were placed on racks at 20 stations
between Manahawkin and Holly Park, New
Jersey, from 1971 to 1980 (Hoagland &
Turner, 1980). One panel was added each
month and removed one month later to de-
termine the timing and rates of larval settle-
ment. One panel was added each month and
removed 12 months later to analyze species
composition, timing of reproduction, lifespan,
sex ratio, population age structure, and the
effects of crowding. Also, 12 panels were
placed at each station in May of each year
and removed, one each month, until none

WOOD-BORING BIVALVES 113

were left. From these cumulative panels,
growth rates, age at maturity, and generation
time could be estimated. In the laboratory, а!
teredinids were removed from the wood,
identified, measured, and examined for larvae
in the gills. Further details of the methodology
are in Hoagland et al., 1977, and Hoagland &
Crocket, 1979.

Population Genetics

Horizontal starch-gel electrophoresis fol-
lowed by staining for specific enzymes was
performed, using the general methods of
Ayala et al. (1973) as applied to mollusks by
Dillon & Davis (1980) and Davis et al. (1981).
Specimens of Teredo bartschi, T. navalis, and
Bankia gouldi were obtained live from wood
panels deployed in the inner coast of Barne-
gat Bay, New Jersey, between Waretown (39°
47.7’ N; 74° 10.9’ W) and Holly Park (39° 54’
N; 74° 8’ W). Specimens of Bankia fimbriatu-
la, Lyrodus floridanus, and Martesia striata
were obtained from panels deployed at the
University of Miami (L. floridanus) and Hobe
Sound, Florida, U.S.A. (B. fimbriatula, M.
Striata). Approximately 50 specimens of each
species were analysed. Voucher specimens
number A8680 a-c and 353444 are on deposit
at the Academy of Natural Sciences of Phila-
delphia. The animals were dissected live from
the wood and frozen in tris tissue buffer (pH
7.4) until used. Preliminary experiments
showed that tissues from various organs
(mantle, siphons, gill, viscera) yielded similar
results though of different intensity, as long as
eggs and larvae were excluded. Therefore,
entire animals were homogenized unless they
were carrying larvae in the gill pouches; in
those cases the gills were excised and dis-
carded before homogenization.

Five wicks of No. 3 Whatman filter paper
were saturated with the homogenate, blotted,

and applied, one wick from each individual, to
each gel. Five gels were run concurrently;
each was then sliced into three slabs. There-
fore one individual could be analysed for 15
enzyme systems. Each population was run on
two days, so that a total of 30 enzyme sys-
tems could be evaluated. As 31 wicks fit on
one gel, 25 experimental individuals from the
population being tested, plus six individuals
from a reference population, could be run on
a single gel.

Starch gels (13%) were prepared using
33.5 9 of Electrostarch and 250 ml of one of
four gel buffers. The buffers were tris citrate
(TC), pH 6.0, tris NaOH borate (Poulik), pH
7.6 (tray buffer)/8.9 (gel), and tris-EDTA-
borate (TEB) at both pH 8.0 and 9.1 (Table 1).
Four systems were run on TEB gels of pH 9
but with tray buffers of pH 8 (TEB 9/8). The
gels were run at 35 MA or 350 volts, but not
exceeding either. Table 2 details the enzyme
systems, their buffer systems, current/voltage
levels, and durations of the runs. No results
were obtained for octopine dehydrogenase,
fumerase, octanol dehydrogenase, succinate
dehydrogenase, or aldolase.

The stain buffers and other components of
the stains are as described by Dillon & Davis
(1980) and Davis et al. (1981). Agar overlays
(10 ml of a 2% solution) were employed for all
enzyme assays except those for AAT,
G3PDH, and LAP, for which solutions were
used. Standard recipes for all systems are in
Shaw & Prasad (1970), Brewer (1970), and
Poulik (1957).

Gels were scored as in Ayala et al. (1973).
The alleles of each locus were identified by
the distance, in + mm, that they migrated with
respect to the most common allele of a refer-
ence population, which was given the arbi-
trary number 100. Teredo bartschi from
Oyster Creek was used as the reference
population because it was nearly monomor-

TABLE 1. Buffers used in gels and electrode trays. Concentration of ingredients (Molarity).

Citric acid
Buffers pH Tris (monohydrate) Boric acid Na2EDTA NaOH

TC Tray 6.0 237 .085 0 0 0

Се! 6.0 .0083 .0030 0 0 0
ТЕВ Тгау 8.0 .500 0 .645 .0179 0

Gel 8.0 .050 0 .097 .0018 0
TEB Tray & Gel 9.1 .087 0 .0087 .0011 0
Poulik Tray 7.6 0 0 3 0 .05

Gel 8.9 .076 .005 0 0 0

114 HOAGLAND AND TURNER

TABLE 2. Enzymes studied, buffers, current, voltage, and duration of electrophoresis.

Enzyme Gel & Tray Buffer Current/Voltage Run time (Hr)
Acid phosphatase (AcPh) TC 6 35 MA 35
Adenolate kinase (Adkin) Poulik 35 MA 3.0
Aldehyde oxidase (AO) TEB 9 350V 4.5
Aspartate amino transferase (AAT) TEB 9 350V 4.5
Esterase NA (EST NA) TEB 9/8 35 MA 2.0
Esterase NP (EST NP) TEB 9/8 35 MA 2.0
Glucose-6-phosphate dehydrogenase (G6PD) TC 6 35 MA 2.0
Glucose-6-phosphate isomerase (СР!) ТС 6 35 МА 2.0
Glutamate dehydrogenase (GDH) Poulik 35 MA 3.0
Glyceraldehyde-3-phosphate
dehydrogenase (G3PD) TEB 8 35 MA 35
a-Glycerophosphate dehydrogenase («GPDH) Poulik 35 MA 3.0
Hexokinase (HEX) Poulik 35 MA 3.0
Isocitrate dehydrogenase (ISDH) TEB 8 35 MA 35
Lactate dehydrogenase (LDH) TEB 8 35 MA 35
Leucine amino peptidase (LAP) TC 6 35 MA 2.0
Mannose-6-phosphate isomerase (МР!) ТЕВ 9/8 35 МА 2.0
NAD-dependent malate
dehydrogenate (NAD-MDh) TC 6 35 MA 3:5
Peptidase G (PepG) TEB 8 35 MA 3.5
Peptidase T (PepT) TEB 8 35 MA 3.5
Phosphoglucomutase (PGM) TC 6 35 MA 2.0
TEB 9 350V 4.5
6-phosphogluconate dehydrogenase (6-PGD) Poulik 35 MA 3.0
Sorbitol dehydrogenase (SoDH) Poulik 35 MA 3.0
Superoxide dismutase (SOD) TEB 9/8 35 MA 2.0
Triose phosphate isomerase (ТР!) ТЕВ 8 35 МА 3:5
Xanthine dehydrogenase (XDH) Poulik 35 MA 3.0

phic and was abundant. Assignment of elec-
trophoretic patterns to loci was done with the
aid of data collected on the same enzyme
systems for other mollusks (Dillon & Davis,
1980; Davis et al., 1981). An electromorph
was not scored if it was found only once.

Calculations were made of: 1) allele fre-
quencies at each locus; 2) A, the average
number of alleles per locus for each popula-
tion; 3) P, the percent polymorphic loci per
population; 4) H, the average individual
heterozygosity; 5) |, Nei’s normalized genetic
identity of genes over all loci; and 6) D, Neïs
genetic distance, or accumulated number of
codon substitutions per locus, between popu-
lation pairs (Nei, 1972; Ayala et al., 1973).
The first value is basic to calculation of the
others. A, P and H estimate genetic variability
within populations, and are used to compare
populations in terms of degree of genetic vari-
ability. Genetic identity (1) and D allow com-
parisons of genetic relationships among pop-
ulations and species. We record fixation of
alternative alleles as well as the allele fre-
quencies in order to note significant genotypic
differences among populations.

Numerical Taxonomy

The morphological data were analysed at
the genus level using Wilson’s consistency
test for phylogenies (Wilson, 1965), a simple
cladistic method. Subsets of taxa were organ-
ized according to shared versus unique and
unreversed character states. In addition, a
phenetic analysis using the NT-SYS numeri-
cal taxonomy program package (Rohlf et al.,
1972) was used, focussing on similarities
among the taxa that may or may not be re-
lated to phylogeny. A data matrix of 146 taxa
(appendix A) and 90 binary or ordered multi-
state characters (Appendix C) was compiled.
Taxa for which insufficient information was
available are listed in Appendix B.

The matrix was standardized by rows
(characters), such that each character had a
mean of O and standard deviation of 1. Both
correlation and taxonomic distance matrices
were generated, and cluster analysis was per-
formed on each, using the unweighted pair-
group method with arithmetic averaging. The
minimum spanning tree (MST) and subsets
subprograms of NT-SYS were used to find

WOOD-BORING BIVALVES

phenetic relationships among the taxa. The
minimum spanning tree configuration is supe-
rior to the phenogram because it does not
average all the relationships between a taxon
entering a cluster and those already clus-
tered.

The standardized data matrix was used to
generate character correlations, which were
subjected to Principal Components Analysis,
with components extracted until the eigen-
values were less than 1.0. A transposed
matrix of the first three principal components
with their character load was post-multiplied
by the standardized matrix to yield a matrix of
operational taxonomic unit (OTU) projections
in principal component space (Rohlf et al.,
1972).

The 146 taxa x 90 character matrix was
used to find correlations among all the char-
acters for the two related families of wood-
borers. Smaller matrices containing first, only
the Pholadidae, and second, only some of the
Teredinidae (Appendix A, numbers in paren-
theses), were used to obtain more detailed
relationships among the taxa, because ana-
tomical characters unique to the family could
be added to the matrix (Appendix C).

RESULTS
Classification and Evolutionary History

An examination of the adaptive radiation of
wood-boring bivalves requires that we cross

115

family lines to consider evolution of all wood-
boring lineages, including those portions of
the lineages that have not adopted the wood-
boring habit. Table 3 shows that obligate
wood- and mud or rock-boring species exist
together in the Pholadidae, while the Teredin-
idae are almost exclusively wood-borers.
From this family structure, we might guess
that wood-boring evolved from mud-boring in
the family Pholadidae. Nonetheless, the fossil
record is insufficient to validate or reject this
hypothesis. Rock-borers are much more likely
to be preserved, because fossilization of
marine wood is relatively rare. For the mo-
ment, we are assuming that the lineages as
expressed by the family structure of the
Pholadacea (Table 3) are correct.

The fossil burrows of wood-boring Marte-
siinae, Xylophagainae*, and Teredinidae can
often be distinguished (Turner, 1969). The
first fossil Martesiinae are suspected from the
Carboniferous, and definitely occur in the
Jurassic (Turner, 1969). Pholadinae also are
suspected from the Carboniferous. The other
pholad subfamilies first appear in the Creta-
ceous; all recognized subfamilies have sur-
vived to the Recent. Most pholad genera are
not recognizable in the fossil record until the
Tertiary, although Martesia, Barnea, and
Xylophaga, representing three subfamilies,
are found in the lower Cretaceous. Xylo-
phoma is known only from the Cretaceous. In
North America, fossil Pholadidae are common
only since the beginning of the Pliocene
(Kennedy, 1974). The fossil genus Teredina,

TABLE 3. Taxonomic position of wood-boring bivalves.

Subclass Heterodonta
Order Myoida
Suborder Pholadina

Superfamily Pholadacea

Family Pholadidae

Subfamily Xylophagainae!*
Genus Xylophaga (Cretaceous-Recent)
Xylopholas (?-Recent)
Xyloredo (?-Recent)
Subfamily Martesiinae2
Genus Martesia! (?Carboniferous-Recent)
Lignopholas! (?-Recent)
Xylophoma! (Cretaceous-?; not Recent)

Family Teredinidae

Subfamily Kuphinae? (?Eocene-Recent)
Teredininae! (Eocene-Recent)
Bankiinae! (Paleocene-Recent)

ТА! members of these groups are obligate wood-borers.

23 of 9 genera are wood-borers.

3Only one genus and species; may be a facultative wood-borer.

"This spelling follows Turner (1969: N721). Xylophaginae is the correctly formed name (1.C.Z.N. Code Article 29(a)) but is a
homonym which should be brought before the 1.C.Z.N. for a ruling (Article 55(a)). ED.

116 HOAGLAND AND TURNER

assigned to the Martesiinae, occurs in fossil-
ized wood in the lower Eocene of Europe
(Wrigley, 1929). It is notable because its
elongate growth form is similar to that of the
Teredinidae.

There are records of tubes associated with
wood in the Jurassic and Cretaceous that
have been assumed to be Teredinidae of
undetermined genus and species (Durham &
Zullo, 1961). However, these tubes could be
Xyloredo. “Teredo” pulchella was named
from material from the Jurassic (Moll, 1942).
Cretaceous teredinids were broadly distrib-
uted; they have been found in Japan (Hatai,
1951), India (Stoliczka, 1871), and North
America (Stephenson, 1952). However,
Teredinidae with pallets preserved and hence
identifiable to genus are known only from the
Paleocene onward.

Pallets of Bankia and Nototeredo have
been dated from the Paleocene (Elliott, 1963;
Cvancara, 1966). The two major branches of
the Teredinidae, the Teredininae and the
Bankiinae, with their distinguishing pallet
types, had diversified by the Eocene (Wrigley,
1929). In fact, pallets attributable to
Nausitora, Bankia, Neobankia, Teredo,
Psiloteredo, and Teredina (a pholad) are all
found in either the London Clay or other
English Eocene deposits (Elliott, 1963), re-
vealing a rich, sympatric fauna of wood-
borers. In addition, Nototeredo and Teredora
are known from the Eocene of France and
Belgium (Vincent, 1925). The Kuphinae may
also have been present in the Eocene, al-
though fossil remains are questionable until
the Oligocene (Moll, 1942), and even then
cannot be positively identified by the tubes
alone.

It appears that both the Pholadidae and the
Teredinidae were world-wide by the Jurassic,
and that most Recent subfamilies and genera
existed by the Eocene. The adaptive radiation
of the Teredinidae was probably very rapid,
as is characteristic of radiation events
(Stanley, 1979).

The modern extent of the wood-borer radia-
tion can be seen in Figs. 1 and 2. In addition,
five fossil genera of Teredinidae have been
described. The greatest diversification has
taken place in Bankia, Teredo, and Xylo-
phaga. Within each subfamily, there are
many genera with low diversity and one with
very high diversity, a few being intermediate.
When the subfamilies are collected into fami-
lies, the pattern is more evident. It is further
strengthened if all the wood-boring members

of the Pholadacea are combined and the
rock-borers are removed (Fig. 2). Ecological-
ly, the radiation is split into the deep-sea
forms (the Xylophagainae) and forms occupy-
ing water less than 250 m deep (Teredinidae
and Martesiinae).

While taxonomic characters апа their
states are listed (Appendix C), the assign-
ment of scores for each taxon is too lengthy to
include here, but forms a separate publication
(Hoagland & Turner, 1981). The Pholadacea
share many characters that clearly are related
to boring in hard substrates. These include
insertion of the anterior adductor muscle on
the umbonal reflection in an exterior position,
so that it works in opposition to the large pos-
terior adductor muscle. Others are a closed
mantle, reduced beak and hinge, a rounded
anterior portion of the shell, a large pedal
gape, denticulate shell sculpture, a discoid
foot, and presence of well-developed internal
shell projections (apophyses, dorsal and ven-
tral condyles, and chondrophore). There is
also a tendency for shell elongation or reduc-
tion and the development of an umbonal-
ventral ridge and sulcus in both families. A
ventral adductor muscle is often present.

Population Genetics

The allele frequencies for 32 loci and the six
species analysed are summarized in Table 4.
Although results were obtained also for pepti-
dase T and esterase NP, these were not as
clear as those obtained for peptidase G and
esterase NA, respectively. Because ester-
ases and peptidases are nonspecific en-
zymes, redundancy would occur if all the data
were scored. Therefore, we do not include re-
sults for peptidase T and esterase NP.

Tables 5 and 6 present the genetic relation-
ships among the taxa based on those 26
enzyme loci for which scorable results were
obtained for all six species. Fig. 3 plots a
dendrogram based on the genetic distances
of Table 6. Clearly, Martesia striata is sepa-
rate, while Bankia forms one group and
Teredo and Lyrodus another within one large
grouping. On the basis of these data, Lyrodus
does not appear to be a separate genus.

Genetic variability for the six species is
shown in Table 7. All 32 loci were used to
calculate these values. The most interesting
result is the correlation between larval type
and level of genetic variability. Over all three
indices, the long-term brooder Teredo
bartschi has low variability, while the spawn-

WOOD-BORING BIVALVES 117

NUMBER OF SPECIES PER GENUS

%,
4
2
e @ =
>
e
J
So
D,
2
e
$,
2
4, .
Y 25
e
a
Sa
%
%
$
e
%, =
+ n
“s
o, №
=
4%
S
o w
oa
a
%
¢ =
>
do
% .
Y
os с
+ р BR cy a
+;
o
4

9, =
%
e 15]

Kuphus

Bactronophorus
Neoteredo
Dicyathifer
Zachsia
Teredora
Uperotus
Psiloteredo
Teredothyra
Lyrodus

3vVaInIa3431l

Teredo

Spathoteredo
Nototeredo

Nausitora

Bankia

Talona
Zirfaea
Cyrtopleura
Pholas

Barnea

Chaceia
Diplothyra
Lignopholas
Aspidopholas
Martesia
Parapholas
Penitella
Pholadidea

3valaV1OHd

Nettastomella

Jouannetia

Xylopholas
Xyloredo

FIG. 1. Patterns of numbers of species per genus in subfamilies of Teredinidae and Pholadidae.

ers Bankia gouldi, В. fimbriatula, and
Martesia striata have high variability. Teredo
navalis and L. floridanus, which are short-
term brooders, are intermediate.

Ecology and Zoogeography

Our population studies of three species
from Barnegat Bay, New Jersey (Hoagland et
al., 1977, 1980; Hoagland & Crocket, 1979)
have shown that the species vary not only in
type of larvae, but in many other population
parameters (Table 8). Teredo bartschi is a
tropical/subtropical species that was intro-

duced to Barnegat Bay (Hoagland & Turner,
1980), so its population parameters may in
part represent its recent past geography. The
evidence from year-long exposure panels is
that Bankia gouldi survives winter tempera-
tures far better than either Teredo navalis
or Т. bartschi. Physiological experiments
(Hoagland, 1981) show that Т. bartschi has a
higher temperature tolerance than either of
the native New Jersey species but has poorer
cold tolerance than B. gouldi. The tempera-
ture tolerances of the three teredinids thus ap-
pear to be in harmony with the natural ranges
of the species.

118 HOAGLAND AND TURNER

WOOD- BORING

TEREDINIDAE PHOLADIDAE PHOLADACEA

COMBINED

NUMBER OF SPECIES PER GENUS

GENERA

FIG. 2. Patterns of numbers of species per genus in families of Pholadacea, and in wood-boring Pholadacea.

TABLE 4. Allele Frequencies.

Locus and Teredo Teredo , Lyrodus Bankia Bankia Martesia
Allele bartschi navalis floridana gouldi fimbriatula Striata
AcPh 98 1.00
100 1.00 1.00 1.00
103 1.00 1.00
Adkin 95 1.00
97 43 .97
100 1.00 .95 57 .03
103 .05 1.00
АО | 85 1.00
97 .43 .29
100 1.00 1.00 57 .71 .85
102 15
AO И 98 .40 =
100 1.00 1.00 1.00 1.00 .60 —
AAT 78 08
80 22
82 70
93 1.00 .86 .05
95 .14 69
97 26
100 1.00 1.00
EST NA I 93 .98
95 .02
100 1.00 .96 .96 .16
103 04 .04 84 1.00
EST NA II 98 .68
100 97 .74 1.00 132
102 .03 .84 .04 .26
103 .08 96

WOOD-BORING BIVALVES 119

TABLE 4. (Continued)

Locus and Teredo Teredo Lyrodus Bankia Bankia Martesia
Allele bartschi navalis floridana gouldi fimbriatula striata
EST NA 111100 1.00 .04 .97 .80
101 .93 .04
103 .07 .20 .40
105 .92 .03
106 60
G6PD 91 1.00
100 1.00 .06 .09
103 94
105 1.00 91
108 1.00
СР! | 100 1.00
102 .30 .05
105 sil .20 54 .70 .50
107 34 .76 .02 .35
109 .04 .07
111 .06 .36 03
115 .09 05
СРЕШ 95 .23 — .06 — =
100 ML 1.00 — .85 — —
105 — 09 = aes
GDH! 99 .07 05 —
100 1.00 .86 1.00 1.00 89
101 .07 05 —
G3PD 97 1.00
100 1.00 1.00 14
103 1.00 .86 1.00
a-GPDH! 98 — .90 —
100 1.00 .91 — .10 —
106 .09 — — 1.00
HEX 91 90
94 10
97 Te .04 .68 .35
100 1.00 .27 96 25 65
102 07
IsDH | 100 1.00 1.00 1.00 1.00 1.00 1.00
IsDH I 95 1.00 —
97 .03 —
100 1.00 .92 .97 .54 —
102 08 —
103 46 er
LDH 97 1.00
100 1.00 1.00 1.00 25
101 1.00 YD
LAP 96 07 07
99 .03
100 1.00 .64 51 .56
102 .10 .02 .26 .44 ae
104 12 .98 .16
105 .04 .28
106 09

108 50

120 HOAGLAND AND TURNER

TABLE 4. (Continued)

Locus and Teredo Teredo Lyrodus Bankia Bankia Martesia
Allele bartschi navalis floridana gouldi fimbriatula Striata
MPI 92 .09 15
94 .19 .70 .66 .65
96 .25 .14
98 .45 .23 it .20 a
100 1.00 li .07 .16
102 74
MDH | 95 .99
(МАО) 100 1.00 1.00 1.00 .01 1.00
101
104 98
109 02
MDH II! 95 — — 1.00
(МАО) 100 57 1.00 — .94 —
102 .43 — —
105 — 06 —
PepG | 100 1.00 1.00 1.00 sz 1.00 1.00
103 66
105 1174
PepG II 100 1.00 25 .03 .21
103 .50 .69 54
105 US 1.00 .16 .06 , .28
107 31 04 12
109 06
PepG Ill 90 .09
93 ail
95 14 .10
98 .24 .66 45
100 1.00 .76 1.00 .37
103 88
104 08
105 12
PGM 95 .02
97 .05 1.00 .09 .08 11
100 1.00 il .09 .50 .09
102 .69 75 08 78
104 15 07 30
106 04
6-PGD 100 1.00 1.00 1.00 .92
101 1.00 1.00
105 08
SoDH 94 .86 .06 .03 1.00
98 .14 .94 .83 .80
100 1.00 .14 .20
SOD | 95 1.00
100 1.00 1.00 .96 1.00 1.00
102 04
106
SOD II 100 1.00 1.00 44 .92 .91
102 1.00 .56 .08 .09
TPI 97 1.00
100 1.00 132 .08 .06
104 1.00 .68 .92 .94
XDH 100 1.00 1.00 1.00 1.00 1.00 1.00

1Enzyme systems with missing data; not used in calculation of genetic distance.

WOOD-BORING BIVALVES 121

Dendrogram of Genetic Distances

Nid < 5
or 2 № 42
oA > e и a
A 3 a yn y? >
Ÿ o o v 4: 4:
О .43
®
= .56
Le]
%
a :13
=
> -88
=
Ф
(0)
1.10
FIG. 3. Dendrogram of genetic distances.
TABLE 5. Genetic Identity Values (I).
Т. navalis L. floridana В. gouldi B. fimbriatula M. striata
T. bartschi .506 .568 .429 .443 .321
Т. navalis .456 .341 375 .290
T. floridanus .460 441 .327
B. gouldi .649 .384
B. fimbriatula .341
TABLE 6. Nei Genetic Distances (D)
T. navalis L. floridana B. gouldi B. fimbriatula M. striata
T. bartschi 0.682 0.565 0.847 0.814 1.135
Т. navalis 0.785 1.077 0.980 1.237
Е. floridanus 0.776 0.818 1.118
В. gouldi 0.433 0.956
В. fimbriatula 1.077
TABLE 7. Genetic variability.
OTE EEE A М A Ss
Percent polymorphic Average number Average individual
loci alleles per locus heterozygosity
(P) (A) (H)
Bankia gouldi .781 2.36 .124
Bankia fimbriatula 61 1.94 195
Martesia striata .56 y 2.03 125
Teredo navalis .50 1.86 .073
Lyrodus floridanus .39 1.55 .042
Teredo bartschi .08 1.08 .003

1.78 = 78%.

122

HOAGLAND AND TURNER

TABLE 8. Relative values of population parameters for three teredinids with different modes of larval

development, in Barnegat Bay, New Jersey.

Parameter
Brooding Absent
No. eggs per reproductive event
Size and stage of offspring at release
Adult body size, uncrowded
Lifespan

Age at first reproduction 3—4 months
Tolerance to crowding Moderate
Sex ratio Skewed to ?
Breeding season Summer
% females with larvae during breed-

ing season ==
Stability of population size Moderate
Adult phoresis Common
Females retain larvae in winter —
Adult winter mortality Moderate
Juvenile mortality Very high
Turnover rate Moderate
Stability of substrate Low
Genetic polymorphism High

The major zoogeographical distinction be-
tween the Pholadidae and the Teredinidae is
that most species of wood-boring pholads oc-
cur in the deep sea, while teredinids breed in
water less than 250 m deep. The major ex-
ceptions are the wood-boring members of the
subfamily Martesiinae, and a few species of
Xylophaga that occur in shallow water. Our
records are not yet sufficient to analyse spe-
cies deployment in the deep sea, but there is
evidence of allopatry among species from the
same group of Xylophaga based on morpho-
logical similarity (Table 9). Those Xylophaga
that do extend into shallow water are found in
high latitudes, e.g. Х. globosa (Chile), Х.
dorsalis, X. praestans, and X. atlantica (N.
Atlantic) and X. washingtona (N. Pacific). In
the deep sea, two to five species of Xylo-
phagainae have been found in a wood panel at
any one station (Turner, unpublished). In
shallow water, rarely is more than one spe-
cies of wood-boring pholad found in a piece of
wood. Yet it is possible to find eight sympatric
species of tropical, shallow-water teredinids
living together, often with a representative of
Martesia.

Data on zoogeography of the Teredinidae
were compiled from Turner (1966, 1971) and
were augmented by more recent investiga-
tions. The division of species according to
type of larvae and geographic range are
shown in Table 10. Long-term larviparous
species tend to occur in only one latitudinal

B. gouldi

Numerous (~ 106)
Small, eggs & sperm
Large (~300 mm)
Several years

T. navalis

Short

Intermediate (—104)
Medium, straight hinge
Medium (~250 mm)
Several years

3—4 months

Moderate

Skewed to 2

Late summer & fall

T. bartschi

Long

Few (—103)

Large, pediveliger
Small (~100 mm)
Usually 1-2 years
6-8 weeks

High

Highly skewed to 2
Late spring to late fall

20-30% Usually 80%
Moderate Low
Common Common

No Yes

High High

High Low
Moderate High

Low Low

Medium Low

TABLE 9. Species subsets within the genus Xylo-
phaga.'

|. Х. concava IV. X. foliata
X. sp. 12 Х. sp. 52
Х. erecta X. atlantica
X. grevei X. abyssorum
X. wolffi X. duplicata
X. lobata
V. X. washingtona
|. Х. galatheae X. rikuensis
X. hadalis X. aurita
X. sp. 22 X. turnerae
X. murrayi
X. panamensis VI. X. globosa
X. africana X. mexicana
X. indica
Ш. X. bruuni X. dorsalis
X. obtusata
X. supplicata Vil. X. praestans
X. sp. 32
X. sp. 42
1Data used to separate the groups are from Turner, in

prep., and Knudsen, 1961. The major characters that
separate the groups are shell and siphon characters
(Hoagland & Turner, 1981).

Turner, in prep.; undescribed Xylophaga.

zone, but in more than one ocean. Planktonic
species tend to be in one ocean, but at wide-
spread latitudes; however, the trend is not
statistically significant.

Of the approximately 70 teredinid species,
over 2/3 are tropical; at least six ofthe tropical

WOOD-BORING BIVALVES 123

TABLE 10. The division of species according to type of larvae and geographical range. The first number is
the observed number of species; the second is the expected number based on the assumption that larval

type and distribution are independent.

Endemic or 1 Ocean

O
Planktonic 25
Short term Larviparous 5
Long term Larviparous 4

Two or more Oceans

= O Е
21.3 7 10.7

6.0 A 3.0

6.7 6 3.3

x2 = 5.70, р < .10 (close to .05)

One latitudinal Zone

Two or more Zones”

Planktonic 28

O
Short term Larviparous 6
Long term Larviparous 10

E O Е
28.5 5 4.5
6.9 2 el
8.6 0 1.4

x? = 2.55, р < .50 (not significant)

A latitudinal zone is defined here as 30° of latitude, starting at the equator.

species are circumtropical. Most of the tem-
perate-zone species are broadly distributed.
The small teredinid genera (those containing
fewer than 6 species) are almost entirely
tropical, and these species tend to be nar-
rowly distributed.

Taxonomic Characters and Taxonomic
Relationships

The raw morphological data were analysed
by the method of Wilson (1965) to produce
cladograms based on derived, and in particu-
lar, unique and unreversed character states
(Figures 4 and 5). Zachsia is omitted because
anatomical data at the genus level are being
revised.

Major morphological characters cannot be
traced through the Pholadacea without involv-
ing loss or repeated evolution of certain struc-
tures (Tables 11-13). For example, accessory
shell plates must be highly convergent (Table
14). The wood-boring habit causes correlation
of such genetically independent and probably
convergent traits as long burrow, the pres-
ence of burrow lining, and often, but not
necessarily, separate siphons. Teredora does
not have separate siphons. The most trouble-
some aspect of Fig. 5 is that it requires the
Jouannetiinae and the Xylophagainae inde-
pendently to lose the apophyses, a structure
which appears functionally advantageous.
Alternatively, the two subfamilies could have

shared a common ancestor (dotted line, Fig.
5). But then, the Jouannetiinae and the
Martesiinae would have to have developed
both the callum and siphonoplax independ-
ently. There is no objective way to choose
between these two alternatives as likely evo-
lutionary sequences without the inclusion of
more characters, including some unique and
unreversed characters. Data on the embryo-
logical development of callum, siphonoplax,
caecum and apophyses in the various sub-
families would also aid in the choice by show-
ing whether they are really homologous in all
subfamilies.

Lyrodus

Psiloteredo Bankia

Neoteredo

Dicyathifer Nausitora

Bactronophorus Spathoteredo

Teredothyra

FIG. 4. Analysis of the Bankiinae and Teredininae
using derived character states.

124 HOAGLAND AND TURNER

Martesia
Lignopholas

Other
Genera Jouannetia

orers Nettastomella

B A

Martesiinae м

Jouannetiinae

Pholadinae

Xylophaga

Xyloredo

Teredininae
Bankiinae

Xylophagainae Kuphinae

FIG. 5. Analysis of the Pholadacea using derived character states.

The major discontinuity in morphology with-
in the Teredinidae occurs between Kuphus
and the other genera (Fig. 5). Kuphus is com-
posed of a single species that lacks the wood-
storing caecum. It shares some characteris-
tics with pholads, but it does have pallets. It
has so many unique features that it must be
considered specialized, yet it is basal within
the Teredinidae because its intestine passes
through the heart. The differences between it
and the other adult Teredinidae emphasize
those characters that are correlated with adult
wood-boring. Adult Kuphus is thought to live
within its thick tube, reaching a length of sev-
eral feet, in decaying wood or in mud. Neither
of the authors have observed live animals in
Situ.

A phenetic analysis of the Pholadacean
data set emphasizes overall similarity of the
various taxa, without regard for actual evolu-
tionary relationships. It allows us to see if
there are interesting correlations among char-
acter states. Our Principal Components
analysis of 52 characters and 72 taxa took 13
components to explain 90% of the variation in
the data. Only the first two components each
explained more than 10% of the variation. The
factor loadings on the first component (43% of
the variation) are in Table 15. Table 16 is a list
of the 24 characters out of 52 that were asso-
ciated with the first Principal Component.
Many of the characters, such as the denticular
ridges on the shell, the very large posterior

adductor muscle, the presence of a calcified
burrow, the gill with single demibranch, the
small labial palps, and the wood-storing
caecum, are associated with wood-boring. In
fact, the first two characters are associated
with wood-boring in all of the major groups of
wood-boring clams: the Teredinidae, the Xylo-
phagainae, and the Martesiinae. However,
some of the characters with high loadings on
the first axis are functionally related to length
of the burrow, and not to wood-boring itself.
Examples are on length of the body, the posi-
tion of the visceral mass relative to the shell,
and the position of the siphonal retractor
muscle on the burrow lining.

Confounding the wood-boring and burrow
length characters of the first component are
characters separating the Pholadidae from
the Teredinidae that are not necessarily relat-
ed to wood-boring. These characters can be
separated from the others according to the
degree that they load onto the first factor axis
(Table 15), because wood-boring pholads join
rock-borers in one set of characters but join
the teredinids in the other set. Characters re-
lated to wood-boring that are unique to the
teredinids have the highest values in Table
15, column 1. Table 17 shows the relationship
between each taxon and the first Principal
Component. Wood-boring species project
negatively because of the particular assign-
ment of numerical values to the traits (Appen-
dix С). The rock-boring pholads and the

WOOD-BORING BIVALVES 125

TABLE 11. Presumed Ancestral and Derived Character States in the Pholadacea.

Pholadacean character states present in all pholadaceans and therefore presumed to have been present in
the ancestral group.

Oo se ON =

Fused mantle

Discoid foot

Pedal gape

Shell with reduced umbo and hinge

Elongate gills (except in Xylophagainae, Jouannetiinae)

Anterior adductor muscle attached at the umbonal reflection of the shell, an exterior attachment site.

Pholadacean character states retained in all the Pholadinae, altered in at least one of the other subfamilies.
These are presumed to be either ancestral or unique by virtue of their evolution after the lineage split.

Gill with 2 demibranchs

Caecum lacking

Short burrow

Shell covers viscera

Posterior adductor muscle about the same size as anterior adductor muscle.
Siphons united

Callum not present

Apophyses

. Non wood-boring

Periostracal lamellae absent

. Mesoplax present (accessory shell plates)

Burrow not lined with calcium
Siphonal retractor muscles attach on the shell
Umbonal-ventral sulcus not well developed

. Weakly denticulated shell sculpture
. Intestine goes through pericardium
. Large ventricular bulb of heart

Derived character states of the Pholadacea (illustrated in Figs. 4 and 5). Traits that were not unique and
unreversed are in brackets.

Branch A: Development of umbonal-ventral sulcus, loss of protoplax

Branch A: Development of wood-storing caecum, long burrow and wormlike body, posterior adductor
muscle enlarged compared with anterior adductor muscle, siphons not completely united, develop-
ment of strong denticulated ridges on anterior portion of shell; one demibranch

Branch B: Development of a callum, siphonoplax

Branch A: Shell is inequivalve, [apophyses lost]

Branch B: Hypoplax, metaplax

Branch A: Evolution of wood-boring habit: [truncated beak of shell], [denticulated shell sculpture]

Branch A: Fringed periostracal lamellae on shell

Branch A: Callum incompletely calcified, [mesoplax lost]

Branch A: Siphonal retractor muscles attached to tube, pallets close the tube, viscera extend in loop
beyond posterior adductor muscle, highly developed dorsal condyles, [loss of mesoplax]

Branch B: [apophyses lost]

Branch A: Siphonal plates with siphonal retractor muscles attached

Branch A: [Periostracal/calcareous burrow lining]

Branch A: Intestine does not go through heart, small ventricular bulb of heart

Branch В: Highly reduced shell, very thick calcareous tube, [caecum lost]

Derived character states in the Bankiinae and Teredininae (Fig. 5).

|.
И.
IN.
IV.

Branch A: Open anal canal

Branch A: Elongate stomach, short intestine

Branch A: Fragmented pallets, approaching a segmented condition
Branch A: Segmented pallets

Branch B: Gills adapted for brooding

Branch A: Periostracal-capped pallets

HOAGLAND AND TURNER

126

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WOOD-BORING BIVALVES 127

TABLE 13. Convergent and Non-linearly evolving Features in the Pholadacea.

1. Brooding
2. Accessory shell plates

3. Callum and Apophyses

4. Labial palps

5. Posterior adductor muscle
6. Stomach shape

7. Heart size and position
8. Caecum

9. Gill shape

10.

Degree of siphon separation

11. Filter-feeding apparatus

Arose independently in Xy/ophaga and Teredininae; structures are dif-
ferent.

Anastomosing pattern of presence-absence in the Pholadidae (Table
14).

One or both of these characters must have evolved more than once in
the Pholadidae. Martesiinae and Jouannetiinae have callum; Jouanneti-
inae and Xylophagainae lack apophyses (Table 12).

Large in rockborers; small in most woodborers. But large in Nototeredo
norvagica; small in Psiloteredo megotara, Bankia gouldi, Teredo
navalis.

Large in all woodborers; reverts (?) to small size in Kuphus.

Globular in most teredinids; elongate in Bankiinae, except for Noto-
teredo, which has a globular stomach. Either Nototeredo’s pallet type
is convergent with Bankiinae, or its stomach type is convergent with the
Teredininae.

Variable in the Teredinidae subfamilies, but usually posterior in the
Bankiinae.

Variable in the Teredininae but large in the Bankiinae. Lacking in the
Kuphinae but present in the Xylophagainae.

In both the Teredininae and Bankiinae, some species have broad gills
while others have narrow gills.

Siphons are separate in Kuphus, but variable within the other subfami-
lies.

Gill-length and degree of siphon papillation are variable in both the
Teredininae and Bankiinae.

TABLE 14. Variability in Accessory Shell Plates in the Pholadidae.

Pholadinae
Siphonoplax no
Hypoplax no
Metaplax no
Protoplax usually
Mesoplax usually
Callum no

Martesiinae Jouannetiinae Xylophagainae
variable yes no
variable no no
variable no no

no no no
yes variable yes
yes variable no

wood-boring teredinids have the highest fac-
tor scores; the pholads project positively and
the teredinids negatively. The wood-boring
pholads with long burrows and the teredinid
Kuphus project weakly negatively while the
wood-boring pholads (e.g., Xylophaga) pro-

ject slightly positively.

The second Principal Component (13% of
the variation) consists mainly of characters
that separate the bulk of the Pholadacea from
Xylophaga, such as lack of faecal pellets in
the burrow, presence of apophyses, long
ctenidia, and a longer incurrent than excurrent
siphon. No new insights are produced by this

information.

A Principal Components analysis of the
Pholadidae alone (78 taxa and 73 characters;
Table 18) allowed entrance into the analysis
of many shell characters lacking in the
Teredinidae, such as shape of the accessory
shell plates. The wood-boring Pholadidae
could be compared with the rock- and mud-
borers. Many of the characters with high
factor loadings on the first axis are related to
wood-boring, but also many are characters
peculiar to the large genus Xylophaga. Wood-
boring Xylophagainae are characterized by a
small crystalline style, stomach, and labial
palps, but large wood-storing caecum. The
shell beak is truncated. Ctenidia tend to be

128 HOAGLAND AND TURNER

TABLE 15. Factor loadings on the first 3 Principal Components explaining 63% of the variance, Pholadacean
morphological data.

Principal Components

1 2 3
Percent of Trace: 42.92% 12.96% 7.03%
Characters
1 Shell size (large)! 0.802 —0.405 0.301
2 Anterior sculpture (ridges) —0.869 —0.294 —0.079
3 Radial ribs 0.888 0.286 0.115
4 Beak shape (truncated) —0.881 —0.304 0.023
5 Valves (asymmetrical) 0.218 —0.016 0.364
6 Umbonal-ventral ridge — 01531 —0.255 0.729
7 Mesoplax present 0.701 —0.421 0.102
8 Posterior muscle scar (sculptured) 0.016 —0.756 —0.152
9 Siphonoplax present 0.416 —0.004 0.490
10 Hypoplax present 0.248 —0.028 0.396
11 Metaplax present 0.379 0.051 0.075
12 Protoplax present 0.476 0.232 —0.688
13 Callum present 0.581 0.083 0.738
14 Apophyses present —0.149 0.821 —0.083
15 Ventral condyle present —0.824 0.185 0.381
16 Dorsal condyle present —0.813 0.434 0.268
17 Posterior concentric sculpture 0.509 0.198 —0.244
18 Posterior ribs 0.220 0.155 —0.416
19 Pedal gape —0.523 —0.223 0.364
20 Adductor muscle attachment (to lamina) 0.129 —0.022 0.246
21 Shell auricle present —0.921 0.326 0.005
22 Pallets present —0.931 0.334 —0.031
23 Calcareous burrow lining —0.886 0.269 —0.078
24 Periostracal burrow lining —0.138 —0.085 —0.029
25 Consolidated faecal pellets 0.117 —0.770 0.008
26 Incur./Excur. siphon width >1 0.469 0.207 0.008
27 Incur./Excur. siphon length >1 —0.118 —0.703 —0.141
28 Incurrent siphon long 0.642 0.026 —0.494
29 Papillae on incurrent siphon 0.208 0.130 0.197
30 Papillae on excurrent siphon —0.230 —0.014 0.267
31 Siphons united 0.703 —0.155 0.102
32 Siphons partially calcareous 0.181 0.058 0.082
33 Visceral ganglion (posterior) —0.931 0.334 —0.031
34 Post. adductor muscle large —0.875 0.025 0.264
35 Post. add. musc. shape (irregular) —0.293 0.119 0.095
36 Adductors close together —0.931 0.334 —0.031
37 Siphonal retractors (on burrow lining) —0.939 0.307 —0.039
38 Ctenidia (long) 0.005 0.962 0.159
39 Number of demibranchs (2) 0.942 0.277 0.123
40 Stomach large 0.909 0.018 0.121
41 Labial palps (large) 0.722 0.382 0.144
42 Wood in gut —0.942 —0.277 = 05123
43 Caecum present 0.847 0.329 —0.098
44 Intestine traverses heart 0.921 —0.326 —0.005
45 Gill position (posterior) —0.942 —0.277 —0.123
46 Sperm transfer (direct) —0.553 —0.386 —0.037
47 Substrate: rock 0.793 0.231 0.235
48 Substrate: mud 0.639 0.275 —0.349
49 Substrate: nuts —0.016 —0.810 —0.005
50 Substrate: wood —0.827 —0.329 —0.002
51 Substrate: live roots —0.139 0.031 —0.009
52 Burrow long —0.861 0.247 0.028

1Parentheses indicate the trait with the highest character state.

WOOD-BORING BIVALVES 129

TABLE 16. Characters associated with the Principal Component of Table 15
explaining 43% of the variation in the Pholadacea data matrix. Characters are
associated at a level of .60 or higher. Characters associated at a lower level

were more highly associated with another principal component.

Shell highly reduced!.2:3
Denticular ridges of shell!

Absence of continuous, prominent radial ribs on shell!

Shell beak truncated!

Absence of accessory shell plates?
Strong ventral and dorsal condyles!
Shell flange present!

Pellets present?

Calcified burrow! 2

Siphons not united for entire length!.2
Posterior position of visceral ganglia?

Posterior position of gills?
Large posterior adductor muscle!

Close positioning of adductor muscles; visceral mass loops posterior to shel£:3
Siphonal retractor muscle inserts on burrow lining?:3

Gills possess 1 demibranch!
Presence of anal canal!
Stomach small!

Labial palps small!

Products of boring enter gut!
Wood-storing caecum!

Intestine does not pass through heart

Body elongate and worm-lik
Long incurrent siphor?

1Characters related to wood-boring.
2Characters related to long burrow.

3Characters unique to the Teredinidae, not necessarily related to wood-boring.

short; the gill is posterior and has only one
demibranch. The wood-boring Martesiinae,
however, have two demibranchs, and lack a
caecum. The Xylophagainae do not have the
gill extending beyond the posterior adductor
muscle; the Martesiinae do. Despite these
important differences, the two subfamilies of
borers have a few similarities. The anterior
shell sculpture of most woodborers is denticu-
late without posterior ribs. The absence of
apophyses and the presence of a pedal gape
tend to be traits of adult wood-borers.

The second Principal Component ex-
plained 11% of the variation, and expressed a
relationship between shell shape and the ac-
cessory shell plates. Correlated characters at
a level above 0.7 were small shell, poorly
developed umbonal-ventral ridge, absence of
a hypoplax, one-piece metaplax (if it is pres-
ent at all), presence of a protoplax, absence
of a callum, solid apophyses in the adult, and
small condyles. One problem in interpreting
this axis is the uncertainty of homology of the
accessory plates given the same name.

The last set of character correlations was
done with a reduced species set of 34
Teredinidae for which detailed anatomical
data were available. There were a total of 61
characters. Eight Principal Components were
required to explain 90% of the variation
(Table 19). Component one separated
Kuphus, thought to be mud-dwelling as an
adult, from the other Teredinidae. Its factor
score was —2.984 on the first component
(Table 20). The characters associated with
the first Principal Component (Table 21) could
be related to the lack of dependence on wood
in older adults. Specifically, the shell of
Kuphus is poorly developed for boring, the
burrow lining is thick enough to withstand
breakage outside of wood, and there is no
wood-storing caecum, at least in the few
specimens that have been dissected.

Component two (15% of the variation)
showed an association of thumbnail-shaped
and sculptured, inflexible pallets with united
siphons and calcareous deposits, especially
rings, in the burrow lining. Other characteris-

130

HOAGLAND AND TURNER

TABLE 17. Factor Scores of Pholadacean Species
on the First Two Principal Components.

Components
Species 1 2

1. Barnea candida 0.812 0.288

2. Barnea parva 0.748 0.215

3. Barnea lamellosa One WAI

4. Barnea subtruncata 0.701 0.201

5. Cyrtopleura costata 0.862 0.352

6. Cyrtopleura lanceolata 0.747 0.143

7. Cyrtopleura cruciger 0.794 0.137

8. Pholas dactylus 0.798 0.138

9. Pholas campechiensis 0.903 0.204
10. Pholas chiloensis 0.828 0.188
11. Zirfaea pilsbryi 0.633 0.154
12. Talona explanata 0.839 0.168
13. Chaceia ovoidea 0.653 0.170
14. Penitella fitchi 0.627 0.102
15. Penitella conradi 0.627 0.102
16. Penitella penita 0.683 0.151
17. Penitella gabbi 0.612 0.118
18. Pholadidea loscombiana 0.790 0.167
19. Pholadidea melanura 0.647 0.133
20. Pholadidea quadra 0.730 0.133
21. Pholadidea tubifera 0.692 0.097
22. Lignopholas rivicola 0.379 —0.032
23. Martesia striata 0.376 —0.165
24. Martesia fragilis 0.483 —0.104
25. Diplothyra smithi 0.588 0.041
26. Parapholas californica 0.748 0.010
27. Parapholas acuminata 0.712 0.010
28. Jouannetia duchassaingi 0.707 —0.066
29. Jouannetia globosa 0.715 —0.096
30. Nettastomella japonica 0.607 0.086
31. Nettastomella rostrata 0.651 0.017
32. Xylophaga dorsalis 0.076 —0.977
33. Xylophaga convexa 0.059 —0.938
34. Xylophaga atlantica 0.041 —1.047
35. Xylophaga washingtona 0.058 —1.174
36. Xylophaga turnerae 0.043 —1.195

Table 17 (Continued)

Components
Species 1 2
. Xylophaga africana 0.003 —0.898
. Xylopholas altenai SOY =.
. Xyloredo ingolfia —0.189 —0.752
. Kuphus polythalamia —0.284 0.128
. Bactronophorus thoracites —0.673 0.114
. Neoteredo reynei —0.613 0.182
. Dicyathifer manni — 07262051871
. Teredothyra dominicensis -0.657 0.136
. Teredothyra matocotana — 0.635 105159
. Teredora malleolus —0.564 0.187
. Teredora princesae —0.564 0.187
. Psiloteredo healdi —0.660 0.117
. Psiloteredo megotara —0.629 0.148
. Psiloteredo senegalensis —0.660 0.117
. Zachsia zenkewitschi —0.756 0.097
. Uperotus clavus 0539081
. Uperotus panamensis — 015390131
. Lyrodus massa —0.690 0.118
. Lyrodus medilobata —0.690 0.118
. Lyrodus floridana — 07287 705117
. Teredo clappi -0.690 0.118
. Teredo furcifera —0.690 0.118
. Teredo navalis —0.728 0.117
. Teredo poculifer —0.690 0.118
. Nototeredo edax — 0.577254 05160
. Nototeredo knoxi —0.625 0.138
. Nototeredo norvagica —0.613 0.204
. Spathoteredo obtusa —0.622 0.141
. Spathoteredo spatha —0.648 0.151
. Nausitora dunlopei —0.661 0.148
. Nausitora fusticula —0.727 0.084
. Nausitora hedleyi —0:7068) 30310
. Bankia australis — 01677 3028
. Bankia campanellata —0.703 0:139
. Bankia gouldi —0:758 01069
. Bankia setacea — 01677 1 05128

TABLE 18. Factor loadings on the first 3 Principal Components explaining 55% of the variance, Pholadidae
morphological data.

Percent of Trace:

Characters
1 Shell size (large)

2 Anterior sculpture (ridges)
3 Radial ribs

4 Beak shape (truncated)

5 Valves (asymmetrical)

6 Umbonal-ventral ridge

7 Mesoplax present

8 Mesoplax divided

9 Mesoplax wrinkled

10 Mesoplax sculptured

11 Mesoplax with tube

12 Mesoplax shape (complex)
13 Posterior muscle scar (sculptured)

Principal Components

1 2
35.52% 10.56%
0.421 —0.661
0.916 —0.001
—0.916 0.001
0.896 —0.173
—0.197 0.256
0.431 —0.560
0.445 —0.466
0.678 —0.037
—0.537 —0.794
0.829 0.058
0.317 0.058
0.533 —0.399
0.686 0.037

WOOD-BORING BIVALVES 131

Table 18 (Continued)

Principal Components

Percent Trace: 35.52% 10.56% 9.21%
14 Siphonoplax present —0.349 —0.291 0.049
15 Siphonoplax calcareous 0.234 0.473 0.076
16 Siphonoplax tube-like —0.220 —0.300 —0.127
17 Siphonoplax sculptured —0.028 0.457 0.079
18 Hypoplax present —0.262 —0.575 —0.032
19 Hypoplax divided —0.054 —0.111 0.053
20 Metaplax present —0.350 —0.320 0.028
21 Metaplax divided 0.040 —0.674 —0.046
22 Protoplax present —0.395 0.530 0.135
23 Protoplax divided —0.006 —0.003 0.010
24 Callum present 0.574 —0.639 0.000
25 Callum sculptured —0.112 —0.511 0.109
26 Callum size (large) 0.008 0.002 0.051
27 Siphonal plate present 0.073 0.089 —0.315
28 Periostracal lamellae present —0.196 —0.397 —0.065
29 Periostracal lamellae divided 0.115 0.107 —0.207
30 Apophyses present —0.854 —0.249 0.014
31 Apophyses solid —0.076 0.698 0.145
32 Ventral condyle present 0.051 —0.793 —0.604
33 Dorsal condyle present —0.584 —0.735 —0.118
34 Posterior concentric sculpture —0.412 0.104 0.006
35 Posterior ribs —0.189 0.295 0.104
36 Pedal gape Е 0.470 —0.208 —0.148
37 Post. adductor muscle attachment (to lamina) —0.109 0.086 0.088
38 Calcareous burrow-lining 0.106 0.115 —0.875
39 Periostracal burrow lining 0.106 0.115 —0.875
42 Consolidated faecal pellets 0.823 —0.238 0.349
43 Incur./Excur. siphon width >1 —0.407 —0.419 0.143
44 Incur./Excur. siphon length >1 0.499 —0.019 —0.155
45 Excur. siphon long —0.526 0.201 —0.045
46 Incur. siphon long —0.302 0.395 0.139
47 Papillae on incur. siphon —0.236 —0.201 0.664
48 Papillae on excur. siphon 0.569 —0.002 0.414
49 Siphons united —0.127 —0.140 0.931
50 Siphons calcareous —0.023 0.038 —0.118
51 Post. add. musc. large 0.471 —0.582 —0.057
52 Post. add. musc. shape (irregular) —0.036 —0.277 —0.203
53 Siphonal retractors (on burrow lining) 0.073 0.089 —0.315
54 Ctenidia (long) -0.982 -0.056 0.097
55 Number of demibranchs (2) —0.982 —0.056 0.097
56 Stomach large —0.947 —0.012 —0.246
57 Labial palps (large) —0.982 —0.056 0.097
58 Wood in gut 0.982 0.056 —0.097
59 Caecum present 0.952 0.072 —0.250
60 Extended excur. canal 0.106 0.115 —0.875
61 Crystalline style (large) —0.955 0.015 —0.289
62 Gill position (posterior) 0.982 0.056 —0.097
63 Accessory genital organ 0.933 —0.008 0.320
64 Vesicula seminalis 0.933 —0.008 0.320
65 Sperm transfer (direct) 0.030 0.071 0.148
66 Larviparity 0.688 0.067 0.270
67 Long-term brooding 0.964 —0.205 0.139
68 Brooding place (gills) —0.805 0.238 —0.110
69 Substrate: rock —0.822 —0.077 0.145
70 Substrate: mud —0.640 0.194 0.082
71 Substrate: nuts 0.948 —0.021 —0.137
72 Substrate: wood 0.929 —0.068 —0.178

73 Burrow long —0.019 0.053 —0.779

132 HOAGLAND AND TURNER

TABLE 19. Factor loadings on the first 3 Principal Components explaining 57% of the variance, Teredinidae

morphological data

Percent Trace:

Characters

1 Shell size (large)
2 Anterior sculpture (ridges)
3 Ventral condyle present
4 Dorsal condyle present
5 Shell auricle present
6 Pallets in cones
7 Pallet cones unfused
8 Pallet with cups
9 Pallet cups: shape (thumbnail)
10 Pallet sculpture (ribbed)
11 Pallet with periostracal cap
12 Pallet with calcareous cap
13 Periostracal awns
14 Calcareous burrow lining
15 Periostracal burrow lining
16 Rings on burrow lining
17 Ridges on burrow lining
18 Incurrent < excurrent siphon width
19 Incurrent < excurrent siphon length
20 Excurrent siphon (long)
21 Incurrent siphon (long)
22 Papillae on incur. siphon
23 Papillae on excur. siphon
24 Siphons united
25 Dorsal lappets present
26 Muscular collar present
27 Large post. add. muscle
28 Stomach (large)
29 Labial palps (large)
30 Caecum (large)
31 Extended excurrent canals
32 Intestine traverses heart
33 Sperm transfer direct
34 Larviparity
35 Long-term brooding
36 2 sexes (dwarf ©)
37 Substrate: mud
38 Substrate: nuts
39 Substrate: wood
40 Substrate: roots
41 Heart large
42 Ventricular bulb (long)
43 Heart posterior
44 Auricles pigmented
45 Mantle thick
46 Gill (long)
47 Stomach elongate
48 Stomach anterior
49 Esophagus long
50 Visceral mass/body ratio high
51 Kidney surrounds intestine
52 Anal canal (closed)
53 Anal papillae present
54 Intestine traverses anal canal

Principal Components

14.67%

WOOD-BORING BIVALVES 133

Table 19 (Continued)

Principal Components

1 2
Percent Trace: 29.57% 14.67% 12.58%
55 Intestine long 0.185 0.496 0.116
56 Intestine over style sac 0.099 0.923 0.159
57 Faecal pellets produced 0.060 —0.349 —0.843
58 Anterior gill section 0.498 —0.560 0.186
59 Gill broad —0.272 0.386 0.624
60 Branchial food groove —0.047 0.028 —0.387
61 Pellets flexible 0.146 —0.622 —0.061

TABLE 20. Factor scores of Teredinidae Species on the First Three Principal Compo-

nents.
Components
Species 1 2 3

1. Kuphus polythalamia —2.984 — 0.113 —0.077
2. Bactronophorus thoracites 0.100 0.291 0.502

3. Neoteredo reynei —0.006 0.474 0.987
4. Dicyathifer manni , —0.061 0.311 0.606

5. Teredothyra dominicensis 0.069 0.234 0.447
6. Teredothyra matocotana. 0.060 0.273 0.522

7. Teredora malleolus 0.095 0.533 —0.399

8. Teredora princesae 0.080 0.548 —0.460

9. Psiloteredo healdi 0.087 0.369 —0.003
10. Psiloteredo megotara 0.121 0.364 —0.266
11. Psiloteredo senegalensis 0.125 0.288 —0.115
12. Zachsia zenkewitschi 0.130 —0.037 —0.047
13. Uperotus clavus —0.173 0.790 —0.680
14. Lyrodus massa 0.131 —0.187 —0.093
15. Lyrodus medilobata 0.158 —0.352 —0.164
16. Lyrodus floridana 0.145 —0.359 —0.191
17. Lyrodus takanoshimensis 0.156 —0.334 —0.116
18. Teredo clappi 0.119 —0.256 —0.167
19. Teredo fulleri 0.138 —0.206 —0.155
20. Teredo furcifera 0.105 —0.288 —0.179
21. Teredo navalis 0.117 —0.238 —0.119
22. Teredo poculifer 0.105 —0.288 —0.179
23. Nototeredo edax 0.086 0.157 —0.032
24. Nototeredo knoxi 0.068 0.219 —0.014
25. Nototeredo norvagica 0.098 0.286 0.061
26. Spathoteredo obtusa 0.101 —0.189 0.062
27. Spathoteredo spatha 0.107 —0.236 0.038
28. Nausitora dunlopei 0.134 —0.277 0.208
29. Nausitora fusticula 0.121 —0.223 —0.018
30. Nausitora hedleyi 0.126 —0.314 0.063
31. Bankia australis 0.099 —0.315 —0.085
32. Bankia campanellata 0.086 —0.250 0.097
33. Bankia gouldi 0.059 —0.397 —0.049

34. Bankia setacea 0.096 —0.277 0.015

134 HOAGLAND AND TURNER

TABLE 21. Characters associated with the first
Principal Component, explaining 30% of the varia-
tion in the Teredinidae data matrix. Characters are
associated at a level of .6 or more.

Shell highly reduced, reduced ear (auricle) on pos-
terior slope!

Shell sculpture reduced!

Ventral and dorsal condyles poorly developed!

Thick burrow lining and mantle!

Long siphons

Muscular collar near siphons!

Small posterior adductor muscle!

No wood-storing caecum!

Extended excurrent canals

Large ventricular bulb of the heart

1Characters possibly associated with reduced ability to
bore into wood in the adult in Kuphus.

tics with high factor loadings on the second
component were a large anterior stomach,
large palps, and long intestine. Genera pro-
jecting positively on the second component
were Uperotus, Teredora, Neoteredo, Psilo-
teredo, Dicyathifer, Bactronophorus, and
Teredothyra (Table 20). The Bankiinae plus
Teredo and Lyrodus projected negatively.
Component three (12% of the variation) re-
vealed a relationship among characters of the
heart, gill, and siphon. These were elaborate
papillae on the excurrent siphon, long gills,
short heart, unpigmented auricles, smooth
burrow lining, and an open anal canal. Taxa
projecting positively and strongly on this axis
were Uperotus, Teredora, and Psiloteredo
megotara.

Similarity of the Pholadidae was assessed
by constructing a minimum-spanning tree dia-
gram of genera (Fig. 6) and one of species
(Fig. 7). Both figures are based on correlation
coefficients, although distance coefficients
gave the same pattern. The correlation of
cophenetic values and the correlation coeffi-
cients was 0.96. The most interesting results
are that the traditional subfamily structure re-
mained intact, while Lignopholas appeared
intermediate between the Xylophagainae and
the Martesiinae.

The species-level analysis (Fig. 7) shows
most genera as tight clusters, although di-
vergence has occurred т Cyrtopleura,
Nettastomella, and Xylophaga. There are
several subsets within Xylophaga. The sub-
sets determined by multivariate analysis of
data from Knudsen (1961) and Turner (in
prep.) are very similar to those determined on
the basis of a few key characters by Turner (in
prep.).

The minimum-spanning tree (MST) of the
Teredinidae was dependent upon whether
correlation coefficients or distance coeffi-
cients were used. This technique is not very
reliable because there are no criteria to use or
choose between the two solutions. The fea-
tures of the minimum-spanning trees that
were conserved in the two methods were a
close relationship between or among: 1)
Dicyathifer, Teredothyra, Bactronophorus,
and Neoteredo; 2) Psiloteredo and Teredora;
3) Teredora and Uperotus; 4) Teredo and
Lyrodus; 5) Bankia, Nausitora, and Spatho-
teredo; 6) Bactronophorus and Psiloteredo;
7) Psiloteredo and Nototeredo; and 8)
Lyrodus and Bankia. In both MST diagrams,
Kuphus was widely separated from the other
teredinid taxa. The link in the MST using coef-
ficients of distance was at 3.38 units, whereas
the next largest distance was 1.45 units.
Lyrodus massa was separated from the other
Lyrodus species because of differences in its
pallets (Turner, 1966). Uperotus clavus and
Teredora princessae were so similar that one
could hypothesize that they belong in the
same genus. Comparing these relationships
with those in Turner (1966, fig. 25), we find
that relationships 1-5 are the same, but 6-8
are different. The phenetic assessment could
be due to either convergences or real phylo-
geny; at least it raises the possibility that
Nototeredo is not closely linked with the other
Bankiinae and that the Bankiinae could be
polyphyletic.

Results of the teredinid data suggested one
other manipulation of the data. All characters
concerning the pallets, except whether or not
they had multiple segments and whether or
not there was a periostracal cap, were re-
moved, in order to see if anatomical data gave
a different phenetic arrangement. The result
was a MST diagram virtually the same as that
with all the pallet data. In both cases, ana-
tomical data such as large intestine, large gill,
position of the heart, and size of the stomach
determined the position of Nototeredo, re-
moved from the other Bankiinae. Therefore
the pallet characters did not alter the phenetic
classification.

DISCUSSION

Taxonomic Characters and Functional
Morphology

A possible sequence in the adaptation of
bivalves for wood-boring is: 1) ability to bore

WOOD-BORING BIVALVES 135

Relationships Among Genera of Pholadidae

FIG. 6. Phenetic relationships among the genera of Pholadidae: Minimum Spanning Tree using Correlation

coefficients.

into hard mud and rock for protection; 2) abil-
ity to bore into wood, which was not available
until woody plants evolved, giving a time di-
mension to the radiation, and 3) ability to use
wood for food. This sequence allows for a
period of adaptation for boring into hard sub-
strate before there was wood. It is logical that
use of wood for food could come only after the
animals could actually inhabit it. The fossil
record is consistent with, but does not prove,
this sequence. The species of Pholadidae
that occasionally occupy wood but do not de-
rive nutrition from it (e.g., species of Barnea)
provide a model for the evolution of wood-
borers within the Pholadacean lineage.

Superfamily-level innovations that allowed
entrance into wood (Table 16) include hinge
reduction, development of inner shell projec-
tions that altered muscle attachment and
hence muscle action, shell elongation, shell
reduction, denticulated shell ridges, a pedal
gape, and the development of a discoid foot.
Some of these characters do not appear in
our numerical taxonomic analysis because all
species in both families have them.

Groups in both families developed the abil-
ity to use wood for food, as shown by the

presence of a wood-storing caecum in both
Xylophaga and the teredinids. Use of wood
for nutrition and filter-feeding are not mutually
exclusive. Many of the taxonomically useful
characters of the teredinids are related to the
degree of filter-feeding: a large gill or elabo-
rate siphonal tentacles, a small caecum, long
intestine, and elaboration of sorting mechan-
isms such as those of the labial palps are
characteristics of filter-feeding. Genera with
the gill extending to the mouth (Uperotus and
Teredora) could represent the ancestral filter-
feeding condition. Nausitora fusticula could
represent a secondary elaboration of filter-
feeding tentacles on the incurrent siphon after
reduction of the gills has occurred in the line-
age.

Probably all species obtain nutrition from
both wood and plankton at some time in the
life of an individual. When the gonad of a
teredinid enlarges prior to reproduction, the
wood-storing caecum may be reduced. Per-
haps then the animals rely on plankton. The
flexibility of feeding is also of critical impor-
tance when crowding occurs and further
growth is impossible. Active wood boring may
cease in favor of filter-feeding under such cir-

HOAGLAND AND TURNER

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WOOD-BORING BIVALVES 137

cumstances. Data are required to test these
suggestions.

It is clear from the extent of the wood-borer
radiation (Figs. 1, 2) that the Teredinidae
have radiated successfully in shallow water,
and the Xylophagainae have done so in the
deep sea. Not enough is known of the deep
sea and the living Xylophagainae to explain
the differential radiation in terms of water
depth, but there are some morphological ex-
planations for the radiation of the Teredinidae.

The relative success of the teredinids is
most probably related to the development of a
calcareous tube and attachment of the si-
phonal retractor muscle to it, together with
elongation of the body and reduction of the
shell. Elongation of the body so that the
viscera extend in a loop beyond the closely-
set adductor muscles has had enormous im-
pact on the anatomical organization of the
Teredinidae, compared with the Pholadidae,
which still resemble the basic bivalve anato-
my (Turner, 1966, figs. 5-11). The result is a
very flexible, wormlike animal that can take
advantage of woody material by twisting and
turning as it grows within it, in a way unavail-
able to any of the pholads but most closely
approached in Xyloredo. ;

Pholads receive protection from added
shelly plates, e.g. the siphonoplax, which are
rather inflexible in closing the burrow when
compared with the tubes and pallets of the
teredinids with their associated musculature.
Have the Xylophagainae been relegated to
the deep sea by competitively superior tere-
dinids, successful only there because of some
physiological character lacking in the tere-
dinids? This speculation has been made for
other groups of deep sea organisms such as
Neopilina, but there are no data on which to
base it.

Many features of the Teredinidae are vari-
able among species, illustrating multiple solu-
tions to a common problem. For example, the
four basic types of pallets are all designed to
close the burrow: simple plugs (Teredo), a
plug plus tube thickenings (Psiloteredo) pal-
lets with flexible periostracal caps (Lyrodus),
and pallets that grow by adding segments of
increasing size at the proximal end (Bankia).
These differences seem representative of
phylogeny, but have no obvious relationship
to ecological differences between the genera.

Other features are highly convergent, being
correlated with similar ecological deployment
of distantly-related species. For example,
mantle and tube thickness are greater in

mangrove and brackish-water species, such
as Kuphus polythalamia, Neoteredo reynei,
Bactronophorus thoracites, and brackish-
water Bankia species (Turner, 1966). These
characters are probably partly under environ-
mental control.

The siphon anatomy of the Pholadidae is
variable at the genus and species levels.
Separate siphons occur more often in wood-
borers. Likewise, the anal canal in teredinids
seems to have a functional relationship with
other characters. It can be closed by a sphinc-
ter in Bactronophorus, Neoteredo, Dicyathi-
fer, and Teredothyra, allowing retention of
loose faecal matter. One might expect a cor-
relation between a closed anal canal and ferti-
lization in the epibranchial cavity, but this
combination did not appear in the numerical
analysis, possibly because of lack of data for
some species. There is a correlation between
well-formed faecal pellets and brooding of
young.

Possible Evolutionary Pathways

Evolutionary pathways for the Pholadacea
have been proposed by several authors
(Turner, 1962, 1966; Purchon, 1941; Knud-
sen, 1961). All were based primarily on analy-
sis of shell and a few anatomical characters.
The computer-generated MST diagrams of
relationships (Figs. 6-7) are not phylogenetic
trees. They show only degrees of similarity
among modern groups, without reference to
ancestors. As alternative hypotheses of an
evolutionary sequence they might be useful,
except that there are several problems with
the technique illustrated by the lack of con-
gruence of MST diagrams of the Teredinidae.
One problem lies in the coding of the data.
There are problems in interpreting covariation
when the linearity of multiple character states
is in doubt. The best use of the phenetic meth-
ods will come when detailed ecological and
life historical data are available for each spe-
cies, so that anatomical similarities and differ-
ences among taxa can be correlated with eco-
logical factors and interpreted functionally.
Then, in comparison with cladistic analyses,
convergences can be identified.

Further application of cladistic methods, on
the other hand, are warranted by the results of
our simple analysis of unique and unreversed
characters (Figs. 4, 5). Our assumption that
wood-borers of the Pholadidae evolved from
a common ancestor in the non-wood-boring
lineage of Pholadidae allowed us to “root” the

138 HOAGLAND AND TURNER

tree at | on Fig. 4. The wood-boring mode of
existence is so specialized that one would ex-
pect strong convergences (or a lack of di-
vergence) between wood-boring lineages.
We still cannot be certain that the Teredinidae
diverged from the Pholadidae after some
pholads became wood-borers, but it is likely
because of the pattern of shared unique and
unreversed characters in the Xylophagainae
and Teredinidae (Table 11). On the other
hand, teredinids could have arisen from
neotenous pholads. For example, Barnea
spp. are well into the substrate before the pro-
toplax develops, and adult Barnea spp. are
often found in wood. The neoteny theory is as
yet untested by embryological data and is not
the simplest explanation, however.

The evolutionary sequence suggested in
Figs. 4 & 5 is harmonious with those based on
our phenetic analysis (Fig. 6) but not with the
belief of Purchon (1941) that the Xylo-
phagainae are derived from the Martesiinae.
Fig. 5 agrees with the phenetic analysis in that
the Pholadinae are most divergent from the
wood-boring lineages.

Our genetic and morphological analyses of
species groups within the Teredinidae (Figs.
3-5) independently suggest that Teredo and
Lyrodus are not more distinct than are many
species within the genus Teredo. However,
unpublished work on embryology by one of us
(Turner) reveals some differences between
some species of Lyrodus and Teredo. Cladis-
tic treatment (Figs. 4, 5; Table 11) and phene-
tic treatment of the morphological data both
suggest that the Kuphinae are not of equal
taxonomic rank with the Bankiinae and the
Teredininae. The method of unique and un-
reversed characters placed Nototeredo far
from the other Bankiinae, despite its seg-
mented pallets (Fig. 5), supporting the hy-
pothesis derived from the phenetic analysis
(Figs. 6-7) that the Bankiinae may be poly-
phyletic. The Bankiinae, the Teredininae, and
the genus Lyrodus are traditionally defined on
the basis of а single character—pallet
shape—and hence could be convergent.
These findings should be used to form hy-
potheses to be tested by molecular genetic
techniques.

Population Genetics

The phenogram constructed on the basis of
genetic distance (Fig. 3) correlates well with
the currently used taxonomic structure of the
Pholadacea. Although no rule exists to de-

lineate taxonomic levels on the basis of ge-
netic distance, our genetic identity and dis-
tance values compare well with the values
cited by Avise (1976) for other organisms, in-
cluding mammals and insects, at the same
presumed taxonomic levels.

One difficulty with the current taxonomic
structure concerns the genus Lyrodus. We
find that L. floridana is very similar to the two
species of Teredo, especially 7. bartschi. As
mentioned above, more data are needed for
other species of Lyrodus to test the validity of
the genus.

The genetic distance values (Table 6) sug-
gest that Martesia striata is distantly related to
all the Teredinidae that we have tested, but is
slightly closer to Bankia than to Teredo. How-
ever, the D values are all so large that the
subtle difference between the distances to the
Bankia and those to the species of Teredo
should not be given any importance. In fact, if
one compares the most common allele for
each locus in Martesia striata versus Bankia
and Teredo (Table 4), М. striata is more sim-
ilar to Teredo than to Bankia at five loci, while
it is more similar to Bankia at only one locus
(peptidase G). If one makes the same com-
parisons but includes only the monomorphic
loci (those with at least 0.95 frequency of one
allele for every species), M. striata is unique
at five loci, is similar to both Bankia and
Teredo at five loci, is similar to Teredo at two
loci, and is similar to Bankia alone at no loci.

The values for genetic variability obtained
in this study (Table 7) are within the range
expected on the basis of earlier work.
Selander (1976) reviewed the literature, and
reported mean P values of 0.587 for marine
invertebrates (0.469 for all invertebrates). The
mean value for our six Pholadacea is 0.487,
0.568 without the unusually monomorphic
Teredo bartschi. Because the Т. bartschi
population used in this analysis is introduced,
it probably has lost genetic diversity due to
founder effects. Recent experiments with
other populations of 7. bartschi show twice as
high a heterozygosity value in a Florida popu-
lation compared with the New Jersey popula-
tion and one introduced into Connecticut
(Hoagland, 1981).

Average H values are 0.147 for marine in-
vertebrates, 0.083 for marine snails (Selan-
der, 1976), 0.084 for the six Pholadacea, and
0.100 for the five pholadacean species omit-
ting Т. bartschi.

The genetic data were analysed for fixation
of alternate alleles within a single population,

WOOD-BORING BIVALVES

evidence of self-fertilization (Selander &
Hudson, 1976). Such evidence was not
found, suggesting that none of the species
examined is exclusively self-fertilizing. How-
ever, many enzyme systems have hetero-
zygote deficiency (Hoagland, in prep.) and
self-fertilization is known to occur in Lyrodus
pedicellatus (Eckelbarger & Reish, 1972).

Teredo bartschi and Lyrodus floridana are
successful colonizers despite their low ge-
netic variability. They fit the “general purpose
genotype” mode of evolution described by
Selander & Hudson (1976) and McCracken &
Selander (1980). These authors state that the
optimal genotype for colonizing individuals
should have great phenotypic plasticity, but
not necessarily great heterozygosity, as
others had previously argued. The impor-
tance of these ideas for evolution is that some
species apparently maintain potential for
broad ecological deployment ма hetero-
zygosity and polymorphism, but another
avenue to the same end is a uniform, nearly
monomorphic genotype that is broadly adap-
tive. This avenue has been documented for
Corbicula fluminea, the Asian clam intro-
duced to the United States (Smith et al.,
1979). We would predict low levels of specia-
tion in such monomorphic taxa.

Ecology and Extent of the Radiation

The pattern of the number of species per
genus (Figs. 1, 2) is reminiscent of the curves
of number of individuals per species in eco-
logical community studies. It has a probabil-
istic basis. It appears that, in a given radiation,
only a few innovations lead to numerous simi-
lar species, whereas numerous lineages sta-
bilize at low diversity. The pattern is based on
different rates of evolution, not on different
ages of the genera, for several of the smaller
genera were fossilized as early as Bankia and
Teredo. Also, it is not based on larval type, for
the three largest genera possess all three
major larval types. The largest genera occupy
all latitudes short of the extreme north and
south where there is no wood.

The ecological extent of the adaptive radia-
tion of the wood-borers can be seen by sum-
marizing the habitats where they are found:
deep sea, open ocean in floating wood, man-
groves, shoreline where wood collects and
where man has added wooden structures,
driftwood in estuaries all the way to essenti-
ally fresh water, and even rhizomes of sea
grass (Zachsia zenkewitschi, recently studied

139

by Turner & Yakovlev (1981). Most species
live in dead wood, but Z. zenkewitschi in-
habits living plant material. It is highly special-
ized, with reduced shell (it bores into very soft
material), a tough, rapidly-secreted mem-
brane that lines the burrow, and a heavy cal-
careous tube. It has separate sexes with
dwarf males living in the mantle pouches of
the female. Dwarf males insure a sperm sup-
ply to the females in their precarious exist-
ence in the rhizomes, which may be torn from
the substrate during storms and which decay
when the plant dies.

No other wood-borers have developed
dwarf males, although this mode of sexuality
would appear to be of advantage. It was once
believed that а! Teredinidae and Xylophaga
were protandrous, but true hermaphroditism
has been found in Lyrodus pedicellatus
(Eckelbarger & Reish, 1972). Xylophaga can
probably store sperm (Purchon, 1941), and
may self-fertilize as may some teredinids, but
more research is needed to confirm self-fertil-
ization. All three modes of sexuality in the
Pholadacea are related to life in temporary
habitats, where isolation of a few individuals
often occurs.

All Bankiinae so far studied have a pattern
of oviparity and planktonic development. All
the Teredininae are larviparous and retain
fertilized eggs, but the length of larval brood-
ing is not even a genus-level character. Many
life history traits tend to be intercorrelated, as
shown in Table 8. All the Teredinidae are
good colonizers and must be opportunistic
because they destroy their own substrate.
Species of the Bankia gouldi type are good
long-distance colonizers, but their populations
are rarely as dense as those with the Teredo
bartschi reproductive pattern. Both species
types have high intrinsic rates of increase and
high competitive ability, B. gouldi by its rapid
growth and large number of offspring, Т.
bartschi by its short generation time and the
high survival rate of its offspring. B. gou/di has
greater gene flow than Т. bartschi, but the
patchy nature of the substrate is still great
enough for reproductive isolation. These cir-
cumstances could explain the high level of
speciation achieved by the genus Bankia,
compared with other teredinid genera (Fig. 1).

The planktonic versus larviparous repro-
ductive pattern does have an effect on distri-
bution (Table 10), but not as strong an effect
as might be supposed. Many long-term larvi-
parous species are constrained to one lati-
tudinal zone, but appear relatively more capa-

140 HOAGLAND AND TURNER

ble of movement across oceans than are
planktonic species. This pattern suggests
some physiological limitation in the larvi-
parous species relative to the other species,
but none is known. Larviparous species dis-
perse in wooden boats and are often trans-
ported to areas unsuitable for their survival.
This must have been the case with Teredo
bartschi, for it was only after two nuclear pow-
er plants established warm-water effluents in
the northwestern Atlantic that populations
spread from the tropics to those areas. There
is no indication that the pattern of dispersal of
adults and larvae changed; only that the en-
vironments became more hospitable.

The success of wood-borers in terms of
numbers of individuals, species, and genera
seems related to the physiological flexibility of
individuals and species, and the phenotypic
plasticity in general, as well as to the oppor-
tunistic life history patterns. Many teredinids
are tolerant of salinities as low as 57 (Blum,
1922). Adults of Teredo bartschi withstand
temperatures from 11° to 35°C. and salinities
from 5 to 45 Yoo in the adult stage (Hoagland
et al., 1980; Hoagland, 1981). Teredinids in
our laboratory have withdrawn the siphons
and remained alive for at least 4 weeks with
little oxygen, and without producing any frass,
indicating that wood-boring has ceased.
Some shipworms have even withstood day-
long freezing, according to observations by
one of us (Turner).

The fact that the virtually freshwater wood-
borers belong to at least four genera (Teredo
poculifer, Nausitora species, Psiloteredo
healdi, and Lignopholas species) in two fami-
lies is indicative of the ecological potential of
the superfamily. Broad physiological tol-
erances help to insure dispersal of individuals
to new sources of wood, because dispersal of
both larvae and adults is in large part passive.
Physiological differences do exist between
species, however, and they help to delineate
species ranges. For example, the introduced
Teredo bartschi has a higher temperature
range (11-35°) than does the native Bankia
gouldi (0-30°С) in New Jersey.

Other examples of teredinid flexibility are
the plasticity of the body size and shape at
maturity and the ability of some species to
filter-feed facultatively. Most species can de-
lay metamorphosis and settlement if no sub-
strate is available. Phenotypic plasticity is a
key feature in the evolution of organisms con-
fined to a substrate; the same pattern is seen
in barnacles and in plants.

One might ask if competition among spe-
cies 15 important in the evolution and ecology
of wood-borers. Competition is important in a
given piece of wood. Fast-growing Bankia
gouldi occlude smaller Teredo bartschi. How-
ever, staggered settlement periods and dif-
ferent modes of larval dispersal may lead to
dominance by one species in one piece of
wood and another in an adjacent piece. Wood
becomes available at irregular intervals, fa-
voring maintenance of several species in
each locality. This temporal instability of the
substrate, plus transport of adults in moving
wooden objects and planktonic dispersal of
some species, allow for the maintenance of a
rich marine borer community.

CONCLUSION

Marine wood-boring bivalves form a classi-
cal adaptive radiation based on innovations of
morphology that allowed entrance into a new
substrate. Fossil evidence indicates that the
radiation was rapid once the innovations oc-
curred. It was a radiation probably spinning off
from that of the rock-boring Pholadidae, and
itself was split quite early into two parts with
different but overlapping sets of adaptations
for wood-boring. In turn, the rock- and wood-
borer radiations created new substrate com-
plexity that has been exploited by other or-
ganisms. The major causes of the divergence
between wood- and rock-borers are derived
from the nature of wood: it is more limited and
temporary than rock and hard mud, although
these, too, fall apart. It is a food source, and
wood newly introduced to water floats, there-
by transporting adult animals.

Morphologically, wood-borers are limited by
their sedentary nature as adults and by the
confinement of their wood-boring habit. Se-
lection pressures for the mechanical aspects
of wood-boring are strong. We expect and
find very conservative shell shape, sculpture,
and adaptations for dispersal that are as
strongly developed as those in parasites,
which also destroy their own substrates.

The radiation of wood-boring bivalves,
based on a patchy, limited, and temporary
resource, has led to patchily-distributed popu-
lations of variable size and stability. The spe-
cies vary in the amount of inbreeding they
have undergone, but potential for inbreeding
is high in most. Isolation, yet the ability of the
Teredinidae and Martesia to disperse as
adults in floating wood as well as in the swim-
ming or crawling larval stage, creates an ad-

WOOD-BORING BIVALVES 141

vantage for either high polymorphism or high
phenotypic plasticity. Isolation plus dispersal
provides a mechanism for a complex world-
wide pattern of speciation.

Natural dispersal plus transport due to
man’s extensive use of wood in the marine
environment has led to the world wide ranges
of single species. In fact, man’s activities may
have reduced the future potential for specia-
tion in the Teredinidae and Martesiinae by in-
creasing genetic exchange among popula-
tions of some species and by spreading spe-
cies that have genetic uniformity such as
Teredo bartschi.

The study of the adaptive radiation of the
wood-boring Pholadacea will profit from
greater knowledge of homologies that will
come from more embryological study. Greater
knowledge of life histories of particular spe-
cies and greater ability to correlate ecology
and natural selection pressures with conver-
gences of morphology are also needed. New
methods of numerical taxonomy show prom-
ise in allowing us to exploit these expanding
data bases.

ACKNOWLEDGMENTS

Biochemical and computing facilities were
made available through G. M. Davis (NSF
grant #DEB 78-01550) at the Academy of
Natural Sciences of Philadelphia. L. Crocket,
C. Hesterman, M. Rochester, J. McKinley,
and J. Harms provided technical assistance.
Numerous residents of Barnegat Bay, New
Jersey, allowed use of their property for field
sites. We were funded by U.S. Nuclear Regu-
latory Commission contract #NRC-04-76-347
to Lehigh University, a Fleischmann Founda-
tion grant to the Wetlands Institute (Lehigh
University), and Office of Naval Research
contracts Nonr-1866 (45), NR104-687, and
N00014-67A-0298-0027 to В. D. Turner, Har-
vard University. G. M. Davis, T. Waller, S. J.
Gould, B. Calloway, and P. Williamson read
and commented upon the manuscript. Collec-
tions at the Museum of Comparative Zoology
(Harvard University) and the Academy of
Natural Sciences of Philadelphia were used in
the course of the study.

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WOOD-BORING BIVALVES 143

APPENDIX A: Jouannetiinae
Table of Operational Taxonomic Units (OTU’s) 35. Jouannetia duchassaingi
36. J. pectinata
Numbers to the left of the species names 37. J. quillingi
are OTU numbers for the comparison of 38. J. globosa
pholads and teredinids using shell and ana- 39. J. cumingii
tomical data. Numbers to the right of the spe- 40. Nettastomella darwinii
cies names, in parenthesis, are OTU numbers 41. N. japonica
for detailed anatomical comparison of the 42. М. rostrata
teredinids alone. Among the pholads, ап Xylophagainae
asterisk indicates that the species is an obli- *43. Xylophaga dorsalis
gate wood-borer. All teredinids except *44. Х. concava
Kuphus polythalamia are obligate wood- *45. X. globosa
borers. Not all known species of Pholadacea *46. X. erecta
were used in the multivariate analysis be- *47. Х. mexicana
cause of lack of detailed information on mor- *48. Х. lobata
phology of some species. Appendix В lists the *49. X. atlantica
species omitted from the analysis. *50. X. galatheae
*51. X. washingtona
*52. X. aurita
Pholadidae *53. X. abyssorum
Pholadinae *54. X. turnerae
1. Barnea candida *55. Х. praestans
2. В. parva *56. Х. panamensis
3. В. lamellosa *57. Х. hadalis
4. В. truncata *58. Х. duplicata
5. В. subtruncata ь *59. X. grevei
6. Cyrtopleura costata “60. X. foliata
7. C. lanceolata “61. X. africana
8. C. cruciger “62. X. wolffi
9. Pholas dactylus *63. X. bruuni
10. P. campechiensis “64. X. tubulata
11. P. chiloensis *65. X. obtusata
12. Zirfaea crispata *66. X. indica
13. Z. pilsbryi “67. Xylopholas altenai
14. Talona explanata “68. Xyloredo пос!
Martesiinae “69. X. пасе!
15. Chaceia ovoidea *70. X. ingolfia
16. Penitella fitchi *71. Xylophaga rikuzenica
17. P. conradi *72. X. supplicata
18. P. penita "73. X, 'Sp. 11
19. P. gabbi "TAX: Sp. 21
20. Pholadidea loscombiana *75. X. murrayi
21. P. melanura "FOX Sp. 31
22. P. quadra “TT. “he Sp: 41
23. P. tubifera “765 X. Sp: D"
*24. Lignopholas clappi Teredinidae
*25. L. rivicola Kuphinae
*26. Martesia striata 79. Kuphus polythalamia (1)
*27. М. fragilis Teredininae
*28. M. cuneiformis 80. Bactronophorus thoracites (2)
29. Diplothyra smithi 81. Neoteredo reynei (3)
30. D. curta 82. Dicyathifer manni (4)
31. Parapholas californica 83. Teredothyra dominicensis (5)
32. P. acuminata 84. T. excavata

33. P. branchiata
34. P. calva ITurner, in prep.; undescribed Xylophaga.

144

114.

Te
I.
if
. T. portoricensis
E
Te

HOAGLAND AND TURNER

. T. matocotana (6)

. Т. smithi

. Teredora malleolus (7)
. Т. princesae (8)

. Psiloteredo healdi (9)
. P. megotara (10)

. P. senegalensis (11)

. Zachsia zenkewitschi (12)
. Uperotus clavus (13)

. U. panamensis

. Lyrodus affinis

. L. bipartita

. L. massa (14)

. L. medilobata (15)

. L. pedicellatus (16)

. L. floridana

. L. takanoshimensis (17)
. Teredo aegypos

. T. bartschi

. T. clappi (18)

. Т. fulleri (19)

. T. furcifera (20)

. T. johnsoni

mindanensis
navalis (21)
poculifer (22)

renschi (may be synonym)
somersi
T. triangularis

Bankiinae

1118:
116.
117:
118.
119:
120.
121.
122;
123.
124.
125:
126.
127.

128.
1129:

130.

131.
132:
133.
134.
135.
136.
137.
138.
1139:
140.

Nototeredo edax (23)
N. knoxi (24)

N. norvagica (25)
Spathoteredo obtusa (26)
S. spatha (27)
Nausitora dryas

N. аиторе! (28)

N. fusticula (29)

N. hedleyi (30)

N. schneideri

N. saulii

Bankia anechoensis
. australis (31)

. barthelowi

. bipalmulata
bipennata

brevis

. campanellata (32)
carinata

cieba

destructa

. fimbriatula

. fosteri

. gouldi (33)

. gracilis

. martensi

DOWN

141. B. orcutti

142. B. philippi

143. B. rochi

144. B. setacea (34)

145. B. zeteki

146. B. neztalia
APPENDIX В:

List of Valid Species Omitted from
Multivariate Analysis

Barnea
alfredensis
australasiae
birmanica
dilatata
fragilis
inornata
manilensis
obturamentum
similis

Pholas
orientalis

Aspidopholas
cheveyi
obtecta
yoshimurai

Teredo
parksi

Penitella
turnerae

Pholadidea
fauroti
kamokuensis
suteri

Parapholas
quadrizonata

Xylophaga
guineensis
japonica
knudseni
tomlini
teramachii

There are approximately 20 taxa of Phola-
dacea which may be valid species in addi-
tion to those discussed in this paper. Many
are Xylophaga spp. (Turner, in prep.).

WOOD-BORING BIVALVES

APPENDIX C:

List of Characters and Character States

used in Multivariate Analysis

Shell Characters

1
12.

14.

19:
16.

~~ gas © №

Shell size
Highly reduced (0)
Reduced, valves cannot cover visceral
mass (1)
Valves cover
(2)

Valves cover whole body (3)

visceral mass only

. Shell sculpture, anterior portion; pres-

ence of denticulated ridges (0, 1)

. Presence of radial ribs and concentric

ridges (imbrications) (0, 1)
Beak truncated (0, 1)

. Valves asymmetrical (0, 1)
. Presence of a well-developed umbonal-

ventral ridge and sulcus (0, 1)

. Mesoplax

Absent (0)
Rudimentary (1)
Present (2)

. Mesoplax division

Not divided (0)

Two pieces (1)

A ventral portion (third piece) present
(2)

. Mesoplax wrinkled (0, 1)
. Mesoplax sculpture

Smooth (0)

Concentric ridges (1)

Cuneiform ridges (2)
Tube extending from mesoplax (0, 1)
Mesoplax shape

Narrow, long (0)

Triangular, transverse (1)

Round or rectangular (2)

Lobed (3)

Semicircular, vertical (4)

Ear-shaped (5)

Longitudinally folded (6)

. Posterior muscle scar

Smooth (0)
Irregular, basically transverse ridges
(1)
Transverse ridges (2)
Transverse to radiating depressions
(3)
Radiating depressions (4)
Herring-bone marks (5)
Siphonoplax
Absent (0)
One (1)
Two (2)
Siphonoplax calcareous (0, 1)
Tube-like siphonoplax (0, 1)

17:

145

Siphonoplax sculpture
Smooth (0)
Pectinate (1)

Spiny (2)

18. Hypoplax present (0, 1)

13:
20.
at:
22.

23.
24.

29:

26.

27.
28.

22:

30.
31.

32.

33.

34.

35.

Hypoplax divided posteriorly (0, 1)
Metaplax present (0, 1)

Metaplax divided posteriorly (0, 1)
Protoplax

Absent (0)

Periostracal (1)

Calcareous (2)

Protoplax divided (0, 1)
Pedal gape closed by callum in animals
that have ceased boring

Callum absent (0)

Callum mostly periostracal (1)

Callum calcareous (2)

Callum sculpture

Mottled (0)

Growth lines (1)

Flutes (2)

Longitudinal ridges (3)

Callum size

Narrow band (0)

Incomplete (1)

Complete (2)

Overlapping (3)

Presence of siphonal plate (0, 1)
Presence of periostracal lamellae

Absent (0)

Posterior slope only (1)

Covers more than posterior slope (2)
Posterior periostracal lamellae divided
(0, 1)

Apophyses present (0, 1)
Shape of apophyses
Short, flattened distally, hollow proxi-
mally (0)
Long, thin, solid (1)
Ventral condyle

Absent (0)

Weak (1)

Moderately well-developed; is reduced

in adult (2)

Highly developed (3)
Dorsal condyle

Absent (0)

Modified umbo, weakly developed (1)

Well-developed (2)

Posterior shell sculpture, concentric

Smooth, growth line only (0)

Foliated concentric ridges (1)
Posterior shell sculpture, other than
concentric

None (0)

Ribs (1)

Ribs extended to form spines (2)

146 HOAGLAND AND TURNER

36. Pedal gape in species without a callum
Absent (0)
Slit (1)
Oval (2)
37. Posterior adductor muscle attached to
special lamina (0, 1)
38. Posterior slope of shell enlarged as a
flange (or auricle) (0, 1)
39. Presence of pallets (0, 1)
40. Pallet constructed as a series of cones;
growth by adding cone elements (0, 1)
41. If cone-type pallet, construction
Short, fused, friable material (0)
Elongate, fused cones (1)
Fused in juvenile stage (2)
Nonfused cones (3)
42. И solid pallet, construction
Unsegmented, solid (0)
Sheath and dagger (1)
Weak ridge partially dividing the pallet
(2)
Cups within a cup at some stage in
development (3)
43. If pallet has cups within a cup,
One (0)
Two (1)
Two as juvenile; thumbnail shape as
adult (2)
44. Pallet sculpture, if pallet is solid type
None (0)
Weakly developed radiating ribs (1)
Well-developed radiating ribs (2)
45. Pallet with periostracal cap in adult (0,1)
46. Pallet with calcareous cap in adult (0, 1)
47. Periostracum on cone-type pallets
Awns absent or poorly developed (0)
Awns smooth (1)
Awns fringed (2)

Burrow Characters

48. Burrow lined with calcium
Absent (0)
Thin (1)
Very thick (2)

49. Burrow lined with heavy periostracum
None (0)
Regular periostracum (1)
Membranous periostracum (2)

50. Calcareous burrow lining: inside de-

posits

None (0)
Material at posterior (1)
Regular rings (2)

51. Calcareous burrow, material at posterior
Concamerations (0)
Posterior division (1)
Posterior longitudinal ridges (2)

52. Burrow filled with consolidated faecal
pellets (0, 1)

Siphon Characters
53. Ratio of siphon widths
Incurrent/Excurrent less than 1 (0)
Incurrent/Excurrent about equal to 1
(1)
Incurrent/Excurrent greater than 1 (2)
54. Ratio of siphon lengths
Incurrent/Excurrent less than 1 (0)
Incurrent/Excurrent about = 1 (1)
Incurrent/Excurrent greater than 1 (2)
55. Excurrent siphon morphology
Absent (0)
Partial groove (1)
Complete groove, smooth lappets (2)
Groove with fringed lappets (3)
Siphon complete, short (4)
Siphon complete, long (5)
56. Incurrent siphon length
Short (0)
Long (1)
57. Papillae on incurrent siphon
Absent (0)
Short, simple (1)
Elaborate (2)
58. Papillae on excurrent siphon
Absent (0)
Short, simple (1)
Elaborate (2)
Clump to one side (3)
59. Siphons united
Siphons separate (0)
Siphons Y to % united (1)
Siphons united except at tip (2)
60. Material imbedded in siphon tissue
None (0)
Chitinous (1)
Calcareous (2)

General Anatomical Characters
61. Dorsal lappets just anterior to siphons
Absent (0)
Tubercles (1)
Present, large (2)
62. Visceral ganglion
Normal bivalve position, surface of
posterior adductor muscle (0)
Posterior, end of pericardium (1)
63. Muscular collar posterior to shell (0, 1)
64. Size of posterior adductor muscle
Small, about equal to anterior adductor
muscle (0)
Larger than anterior adductor muscle
(1)
Very large shell modified in area of at-
tachment (2)

65.

66.

67.

68.

69.
70.

Zi.
we

73.

74.

75.
76.
tks

78.

29,

80.

81;

82.

83.

WOOD-BORING BIVALVES

Shape of posterior adductor muscle

Round (0)

Oval, elongate (1)

Irregular (2)

Relative position of posterior and ante-
rior adductor muscle

Far apart (0)

Close together, visceral mass extends
in a loop beyond posterior adductor
muscle (1)

Insertion of siphonal retractors

On shell valves (0)

On siphonal plates (1)

On burrow lining (2)

Ctenidia length

Short (0)

Long (1)

Number of demibranchs, gill (1, 2)
Stomach size (relative to body size)

Small (0)

Medium (1)

Large (2)

Size of labial palps

Small, attached (0)

Large, free at ends (1) |
Products of boring enter gut (0,1)
Wood-storing caecum

Absent (0)

Small (1)

Medium (2)

Large, gonads dorsal to it (3)
Extended excurrent and/or incurrent
canals (0, 1)

Intestine traverses heart (0, 1)
Large crystalline style (0, 1)
Gill position

Before posterior adductor muscle (0)

Beyond posterior adductor muscle (1)
Presence of accessory genital organ
(0, 1)

Presence of Vesicula seminalis (0, 1)
Type of sperm transfer
Free-spawning; fertilization external

Female sucks in sperm (1)
Pseudocopulation (2)

Larval type
Oviparity (0)

Larviparity (1)

If larviparous,

Short-term brooding (0)
Long-term brooding (1)

If larviparous, brooding method
In burrow, on back of shell (0)
At base of siphons (1)

In mantle cavity (2)
In gills (3)

84.

147

Sex
Protandrous (0)
Dwarf male (1)

Ecological Characters

Sas

. Burrows in rock (0, 1)
. Burrows in mud, clay, peat (0, 1)
. Burrows in nuts, seeds, husks, jute

(0, 1)

. Burrows in wood (0, 1)
. Burrows in living roots (0, 1)
. Burrow length

Short (0)
Long (1)

Lives in full ocean salinity (>25%.)
(0,1)

Lives in brackish water (0, 1)

Lives in fresh water (<4°%) (0, 1)

Detailed Anatomical Characters, Reduced
Species Set (Teredinids)

94.

95:

96.

97.

98.

100.

101,

102.

Heart size/body size (ratio)
=.2 (0)

3 5)
[85 29,12)

Size of ventricular bulb
Short (0)

Long (1)

Heart position
Anterior (0)

Median (1)
Posterior (2)

Pigmentation of auricles
Not pigmented (0)
Lightly pigmented (1)
Heavily pigmented (2)

Mantle thickness
Thin (0)

Thick (1)
Very thick (2)

Ratio of gill length/body length
Short, to .2 (0)
Medium, .3 — .5 (1)
Long; .6.— «1 (e)

Almost the length of the animal, .8 — .9

(3)

Shape of stomach
Globular (0)
Intermediate (1)
Elongate (2)

Position of stomach
Posterior (0)

Anterior (1)

Esophagus long (0, 1)

148

103.

104.
105.

106.
107.
108.

HOAGLAND AND TURNER

Ratio of visceral mass to body length

<.2 (0)
3/55 (1)
6-90)

Kidney surrounds intestine (0, 1)
Anal canal
Absent (0)
Open (2)
Closed (2)
Anal papillae (0, 1)
Intestine travels down anal canal (0, 1)
Length of intestine
Short (0)
Moderately long (1)

109.
110.

м
ire

113.

Very long (2)

Many extra coils (3)
Intestine loops over style sac (0, 1)
Production of faecal pellets (0, 1)
Gill with anterior portion (0, 1)
Gill width

Blade-like, narrow (0)

Broad and flat (1)
Branchial food groove well-developed,
(0, 1)

Ecological Characters, Reduced Species
Set (Teredinids)

114.

Pallets flexible (0, 1)

MALACOLOGIA, 1981, 21(1-2): 149-176

VARIATION IN SHELL SHAPE AND SIZE OF HELICID SNAILS IN RELATION

TO OTHER PULMONATES IN FAUNAS OF THE PALAEARCTIC REGION

A. J. Cain

Department of Zoology, Liverpool University, Liverpool L69 3BX, England

ABSTRACT

A study is made of the distribution of values of shell height h and maximum breadth d in the
family Helicidae, which is the most variable in these characters in the Palaearctic fauna. In most
terrestrial gastropod faunas, plotting h against d gives two separate scatters, the upper one
corresponding to high-spired shells, the lower to equidimensional to discoidal ones. The vast
majority of the Helicidae are in the lower scatter, with a few in the upper. Scatters for the
separate subfamilies and other major subgroups show that when such groups coexist, they
either differ markedly in average shell size or, if their size-ranges coincide, they differ in local
habitat.

A survey of separate faunas from the Atlantic islands through Europe and the U.S.S.R. to the
Pacific shows that, except in some islands and in the Far East, the Helicidae are accompanied
throughout by much the same suite of other families which complete the two scatters, each
occupying a characteristic area within them. Where in the Atlantic islands there is a poor
representation of small-shelled species of other families, the Helicidae produce a number of
small species. In the Central Asian mountains, the larger shells of the lower scatter are a mixture
of helicids and bradybaenids, and in the Maritime Territory of the U.S.S.R. all the larger shells
are of bradybaenids, the few helicids being medium-sized. In this region the Palaearctic and
Oriental faunas meet, and the ecological and historical interpretation of replacement of Helicidae
by Bradybaenidae is discussed. Within the continental faunas generally, variation in major
subgroups seems to correspond to overall ecological differences in different regions with the
possible exception of hygromiines and helicellines; the restriction of the scatters in steppe,
tundra, and regions with highly continental climates is discussed. The sporadic production of
high-spired forms occurs in coastal districts of the Mediterranean (several helicellines), on Porto
Santo, on Santa Maria (Azores), and in the Austrian Alps. The coastal forms seem to be in a
habitat without other tall shells. The others are presumably also filling vacant niches.

Comparison of the family Helicidae with families in other faunas suggests strongly that its
comparative constancy in shell proportions is caused by competition from the rather uniform
suite of other families that accompany it, not by any evolutionary or physiological constraints.

INTRODUCTION

It has been shown elsewhere (Cain, 1977a)
that the distribution of shell height and
breadth in free-crawling, fully terrestrial gas-
tropods which can retract completely into their
shells—i.e. excluding slugs and semi-slugs—
is not random but shows a consistent pattern.
In the Stylommatophora (and indeed in land
prosobranchs in most faunas: Cain, 1978b) a
scatter diagram of maximum shell height, h,
against maximum shell breadth, d, gives two
main scatters corresponding to high-spired
shells and to equidimensional to discoidal
shells, with a gap between them at all shell
sizes. These two scatters are found in faunas
as taxonomically different as those of western
Europe, eastern North America, Puerto Rico,

New Caledonia, the former Belgian Congo
(Cain, 1978b), and, with only partial excep-
tions, the Philippines and the New Guinea re-
gion (Cain, 1978a). Some pulmonate families
are found only in the upper scatter (of tall
shells), some only in the lower, but several
have a few or many representatives in both.
There are strong indications that within a
fauna families tend to be mutually exclusive
within a scatter, each occupying a definite
area and combining with the others to fill up
the scatter area (Cain, 1977a). This suggests
some form of interaction between groups,
probably competition. Some _ taxonomic
groups may overlap within a fauna. However,
at least in the western European fauna, they
tend to occupy different habitats, or perhaps,
as in the case of the partly carnivorous zo-

(149)

150

nitids, they may be taking different food. Few
or none are food specialists to the same ex-
tent that so many insects are found to be.

The suggestion that such food generalists
may avoid competition by feeding preferenti-
ally on surfaces of different inclination, and
that shell shape is at least partly adapted for
locomotion at different angles (Cain, 1977a) is
supported by studies on the British fauna
(Cain & Cowie, 1978; Cameron, 1978). Ona
larger scale, families or other groups should
show replacement by each other in the scatter
diagrams of different faunas. The purpose of
this paper is to determine the variation in h
and d of the family Helicidae, in both conti-
nental and insular faunas.

MATERIALS AND METHODS

Measurements of helicid shells for this pa-
per were taken from representative speci-
mens in the collections of the Academy of
Natural Sciences of Philadelphia, and are
those specified by Cain (1977a). They were
supplemented by those of the British Museum
(Natural History) and checked against the lit-
erature. Considering the variation in h and d
within most species, slight differences in the
modes of taking measurements are highly un-
likely to introduce any perceptible bias in such
a survey as this. The Academy collections
contain many lots from the Lowe-Wollaston
collection of Macaronesian shells, and from P.
Hesse’s European collection which were
themselves originally collected by Pallary,
Bourguignat and others. The vexed question
of the validity of specific limits (especially with
Bourguignat’s material, see Dance, 1970)
remains unsettled for want of a biological ap-
proach made on well-localised live material,
and has prevented an adequate examination
of North African faunas. Since it is at any rate
likely that species which are the types of gen-
era, subgenera and sections are valid spe-
cies, these are marked specially in Figs. 1-9
which show variation in h and d in major
groups within the helicids. The other species
can be seen to cluster around them, few being
aberrant. It is probable, therefore, that particu-
lar scatters do show an adequate representa-
tion. But while emphasis is put on the area
occupied by a scatter, little is put on the exact
number of points within the scatter. While in a
few faunas the points shown may represent a
nearly complete enumeration of the species
present, in most they are only a sample.

CAIN

For helicid species not available to me, and
those of other families, mean measurements
have been taken from the data given by
Likharev & Rammel’meier (1962), brought up
to date by the monograph of Shileyko (1978a)
on the Helicoidea. Wollaston (1878) and
Nobre (1931) were used for the Madeiran
archipelago, Mandahl-Barth (1943) being fol-
lowed for the Madeiran helicids. Backhuys’s
excellent monograph (1975) was used for the
Azores, and various scattered papers for the
Canaries.

The classification of higher groups used is
that of Taylor & Sohl (1962), but more sub-
groups of the Helicidae are used than are
recognised by them or Thiele (1931). The
purpose of this is simply to ensure that groups
that might have ecologically distinctive char-
acters are recognised, and that heterogene-
Ous groups are not lumped together; there is
no intention of expressing any taxonomic
judgment on their rank.

The classification of the Helicidae is, at
present, in a state of change. Watson (1943)
remarked in passing that there was a curious
correspondence between the genera of the
helicellines and the hygromiines, but he left
them as coordinate groups. Shileyko (1978a,
b) brings forward convincing evidence that the
helicellines are derived polyphyletically from
the hygromiines. He separates the helicodon-
tines as a distinct family, with the Helicodon-
tinae and the new Lindholmiolinae as sub-
families, removes to the hygromiines a num-
ber of species from the Bradybaenidae, and
elevates the hygromiines to a family, with sub-
families Trichiinae, Hygromiinae, Archaicinae
(new), Euomphaliinae (new), Paedhoplitinae
(new) and Metafruticicolinae. The helicelline
genera Helicopsis, Xeropicta and Helicella
are in the Trichiinae, Cernuella and Xerosecta
in the Hygromiinae; Monacha is in the
Euomphaliinae. Perhaps more surprising is
the transfer to the Polygyridae of /sognomo-
stoma subpersonatum (Midd.), which occurs
near the sea of Okhotsk.

In the present paper, | have retained the
Helicodontidae and Hygromiidae as subfami-
lies of the Helicidae in its more usual sense,
and left the helicellines separate since their
ecological habits are distinct. The following
subgroups of the Helicidae are therefore
used: Hygromiinae, Helicodontinae, Lep-
taxinae, Helicigoninae (Ariantinae in
Shileyko), Monachines (for Monacha and its
subgenera or allied genera), Sphincterochili-
nae, Geomitrinae, Helicellinae and Helicinae.

PALAEARCTIC HELICID SHELLS 191

Murella and Tacheocampylaea, considered
as subfamilies by Germain (1930), are includ-
ed in the Helicinae.

VARIATION WITHIN SUBFAMILIES AND
OTHER GROUPS OF THE HELICIDAE

The family Helicidae is distributed naturally
in the Palaearctic region including Africa north
of the Sahara, with one genus, Lejeania, iso-
lated in the Abyssinian highlands. Eastwards
it ranges into Mesopotamia and Persia and
the Central Asian mountains, from the Kopet
Dagh to the Tien Shan, with a few stragglers
into Siberia and across to the Pacific (Hy-
gromiinae: Zenobiella rubiginosa and 2.
nordenskioldii to the Maritime Territory of the
U.S.S.R., Perforatella bicallosa to the Altai, Р.
gerstfeldti to the Lake Baikal district and Мап-
time Territory). To the west, one species only
(Helicinae: Cepaea hortensis) may perhaps
be a native of the north-eastern coast of the
U.S.A. The family is well represented in the
Macaronesian Islands (Azores, Madeira
group, Canaries and Cape Verdes) in which
there are two endemic subfamilies, the Lep-
taxinae and Geomitrinae, and various en-
demic genera in other subfamilies. A series of
oceanic faunas is therefore availble to com-
pare with the continental ones.

Figs. 1-9 show the h, d scatters for all the
subgroups of the Helicidae. All are wholly or
predominantly within the lower scatter, but in
the Leptaxinae (Fig. 3), Helicigoninae (Fig. 4)
and Geomitrinae (Fig. 7) a single species is
high-spired. In the Helicellinae (Fig. 8) seven
are well across the bisector (the line on which
h = d), and another five cross it but could be
considered part of the principal cluster. In the
Leptaxinae, the high-spired species is Helix-
ena sanctaemariae in the Azores; in the
Helicigoninae it is Cylindrus obtusus in the
Austrian Alps; in the Geomitrinae it is Discula
(Hystricella) turricula in Porto Santo (Madeira
group). The principal high-spired helicellines
are the three species of the genus Cochli-
cella, on Mediterranean and Atlantic shores of
Europe and North Africa. The remainder are a
scattering of species in Candidula, Cernuella
and (mainly) Trochoidea in the Mediterranean
region. Apart from the various helicellines,
therefore, the clearly high-spired helicids are
geographically and taxonomically isolated—
there is no one region in which helicids tend to
be high-spired.

The vast majority of the helicids, then, be-

long to the lower scatter. The Helicinae (Fig.
9) are unique in that they appear to be hetero-
geneous in h, d with one subscatter well into
the lower scatter area and somewhat below
the bisector (i.e. it is of slightly to markedly
depressed shells). A second subscatter which
runs along and slightly above the bisector and
On average is composed of larger shells.
These are in fact the species of the genus
Helix itself, with its numerous subgenera.
(The type-genus, as is not unknown else-
where, is therefore somewhat abnormal in the
family.) The Helicinae are generally large for
the family, with values of d from about 15 to
about 50 mm. In most other subgroups (ex-
cept for a few comparatively giant species) d
ranges from 5 to 25 mm, but the Helicigoni-
nae (Fig. 4) range from 10 to 35 mm and the
Sphincterochilinae (Fig. 6) from 13 to 30 mm.

FIG. 1. Scatter-diagram for h (shell height) and d
(maximum breadth) for the Hygromiinae. Each
symbol gives h and d for adult shells of a single
species. Black circles, type-species of genera, sub-
genera or sections. Both axes marked at 5mm
intervals.

FIG. 2. Helicodontinae; h, d scatter diagram. Sym-
bols as in Fig. 1.

152 САМ

FIG. 3. Leptaxinae; h, d scatter diagram. Symbols as in Fig. 1.

FIG. 4. Helicigoninae; h, d scatter diagram. Symbols as in Fig. 1.

PALAEARCTIC HELICID SHELLS 153

The abundance of rather small shells in the
family is clear in Fig. 10. This gives the scatter
for the whole of the Helicidae, and empha-
sizes again the peculiarity of the large shells
along the bisector (Helix s. |.). The bulk of the
symbols lie clearly below it except for the
helicelline small shells that trespass across.

Overlap between the subgroups of the
helicids is therefore extensive. The major
parts of the scatter areas occupied by the
hygromiines, helicellines, leptaxines and
helicigonines are coincident, and the heli-
codontines, geomitrines, monachas and
sphincterochilines coincide with this principal
area. Of these groups, the leptaxines and
geomitrines are Macaronesian, occurring to-
gether in abundance in the Madeira group
and showing less overlap in their scatters
than each does with other subgroups. The
sphincterochilines inhabit hot arid country
where they coincide with some helicines,
usually of larger size, and with some heli-

FIG. 5. Monacha and related genera; h, d scatter
diagram. Symbols as in Fig. 1.

FIG. 6. Sphincterochilinae; h, d scatter diagram. Symbols as in Fig. 1.

154 CAIN

FIG. 7. Geomitrinae; h, d scatter diagram. Symbols as in Fig. 1.

FIG. 8. Helicellinae; h, d scatter diagram. Symbols as in Fig. 1.

PALAEARCTIC HELICID SHELLS 195

SS nf en le ee

FIG. 9. Helicinae; h, d scatter diagram. Symbols as in Fig. 1.

cellines which are usually smaller. Of the rest,
helicodontines and most helicigonines are
montane or alpine; helicodontines are, on
average, notably the smaller. In western and
central Europe, the hygromiines, the Mona-
cha group (which taxonomically is placed with
them), and the helicellines occur together and
are of much the same size range; the heli-
cines with which they coincide are markedly
larger. The similar forms, however, differ in
habits (and colour pattern correspondingly:
Cain, 1977b). The helicellines sit out during
the day in very open habitats exposed to sun.
Monachas are perhaps intermediate. Hy-
gromiines prefer more densely vegetated,
shadier and damper places and do not sit out.

Some hygromiines, however, in the south of
Europe and apparently in regions further east
stand as much exposure as monachas and
probably as helicellines. The greatest abun-
dance of helicelline species is in the Mediter-
ranean region, and elsewhere hygromiines
probably take on their habits and colour-pat-
terns. This is suggested strongly by some of
the pictures in Shileyko (1978a) and made
explicit by Shileyko (1978b), and it is hoped
that Russian workers will give some further
account of the ecology and habits of the
abundant hygromiine species of the Caucasus
and further east.

Unfortunately, not too much has been re-
corded of habits and habitats of many Euro-

156 CAIN

pean snails, either. The necessarily very gen-
eral remarks just made do suggest, however,
that subgroups coinciding geographically
either differ in average shell size or take up
different habitats.

The general distribution of h and d within
the family as a whole now needs examination
in relation to those of the other families with
which the Helicidae coincide. Cain (1977a:
338-390 and figs. 6-8) has shown that in
western Europe, although the subgroups of
the Helicidae overlap widely with each other,
they overlap very little with the accompanying
families which are themselves mostly mutual-

d
FIG. 10. Scatter diagram (h, d) for all the Helicidae. Symbols as in Fig. 1.

ly exclusive in h, d. The question now is
whether this is true over the rest of the heli-
cids’ range.

VARIATION WITHIN OTHER FAMILIES

An inspection of the figures in Germain's
volume (1930) on the terrestrial malacofauna
of France, and similar monographs, is enough
to show that the other families of pulmonates
in the regions of the Palaearctic considered
here are much less variable in h, d than are
the Helicidae. They are listed below with their
variation in shell shape.

PALAEARCTIC HELICID SHELLS 157

Suborder ORTHURETHRA
Superfamily Cionellacea
Cionellidae (= Cochlicopidae)
Pupillacea
Pyramidulidae
Vertiginidae
Orculidae
Chondrinidae
Pupillidae
Valloniidae
Valloniinae
Acanthinulinae
Strobilopsinae
Enidae
Chondrulinae
Jaminiinae
Eninae
Napaeinae

Suborder MESURETHRA
Superfamily Clausiliacea
Clausiliidae
Clausiliinae
Phaedusinae
Cochlodininae

Suborder HETERURETHRA
Superfamily Succineacea
Succineidae .

Suborder SIGMURETHRA
Infraorder Holopodopes
Superfamily Achatinacea
Ferussaciidae
Subulinidae
Infraorder Aulacopoda
Superfamily Endodontacea
Endodontidae
Punctinae
Discinae
Arionidae
Superfamily Zonitacea
Vitrinidae
Zonitidae
Vitreinae
Zonitinae
Gastrodontinae
Daudebardiinae
Parmacellidae, Milacidae, Limacidae,
Trigonochlamydidae
Superfamily Ariophantacea
Euconulidae
Ariophantidae
Superfamily Testacellacea
Testacellidae
Infraorder Holopoda
Superfamily Polygyracea
Polygyridae
Superfamily Oleacinacea
Oleacinidae
Superfamily Helicacea
Bradybaenidae
(Helicidae)

tall shells only
moderately depressed
rather tall to tall

tall only

tall to very tall
subglobular to depressed
very depressed
subglobular to depressed
depressed

tall only

very tall only

omitted (semiaquatic)

tall
very tall, but decollated

depressed only

omitted (slugs)

somewhat depressed
depressed

omitted (slugs)
omitted (all slugs)

somewhat depressed
depressed

omitted (slugs)

here, depressed
tall here

subglobular to depressed here

158 CAIN

| d
FIG. 11. Russian Carpathians; h, d scatter diagram for the pulmonate fauna. Axes marked at 5 mm intervals.

Symbols for Figs. 11-24:—
Suborder ORTHURETHRA, diamonds.
Cionellidae, all black. Pyramidulidae, black bar left upper side. Vertiginidae, black bar right upper

side. Orculidae, circle in centre. Chondrinidae, horizontal line. Pupillidae, vertical line. Valloniidae:
Valloniinae, oblique line sloping down to left; Acanthinulinae, oblique line down to right; Strobilopsi-
nae, black cross. Enidae: Chondrulinae, black oblique bar down to right; Jaminiinae, black vertical
bar; Napaeinae, black oblique bar down to left.
Suborder MESURETHRA, squares.
Clausiliidae: Clausiliinae, all white; Phaedusinae, all black; Cochlodininae, speckled.
Suborder HETERURETHRA omitted (Succineidae, semi-aquatic).
Suborder SIGMURETHRA
Infraorder Holopodopes, crosses
Ferussaciidae, oblique cross. Subulinidae, vertical cross.
Infraorder Aulacopoda, triangles.
Endodontidae: Punctinae, central black dot; Discinae, central circle. (Arionidae omitted, slugs).
Vitrinidae, two vertical lines. Zonitidae: Vitreinae, speckled; Zonitinae, all white; Gastrodontinae, 3
black dots. (Daudebardiinae, Parmacellidae, Milacidae, Limacidae, Trigonochlamydidae all omitted,
slugs). Euconulidae, black bar, right side. Ariophantidae, black bar, left side. (Testacellidae omitted,
slugs).
Infraorder Holopoda, circles.
Oleacinidae, with circle inscribed. Bradybaenidae, all black. Helicidae: Helicellinae, all white;
Geomitrinae, central black dot; Hygromiinae, left half black; Monacha group, right half black;
Helicodontinae, right lower half black (oblique); Helicigoninae, left lower half black (oblique);
Leptaxinae, upper half black; Helicinae, lower half black; Sphincterochilinae, 4 black dots.

PALAEARCTIC HELICID SHELLS 159

VARIATION WITHIN THE
PALAEARCTIC REGION

(i) Continental regions
(a) Europe

The deployment with respect to h and d of
the Helicidae and other families in the Russi-
an Carpathians is shown in Fig. 11, which
agrees well with that given by Cain (1977a)
for western Europe. Both are or were forested
regions, with montane habitats, and, in the
southern part of western Europe, both experi-
ence a Mediterranean climate, hot and dry
throughout the summer. In Fig. 11, by com-
parison with western Europe, large helicines

are rather few, and zonitids, clausiliids, enids
about the same. Hygromiines are rather well
represented, as would be expected from a
forested region, and helicellines proportion-
ately few. There is little variation, therefore, in
distribution of h and d and taxonomy from
Oceanic western to continental eastern
Europe at the family and major sub-group
level, except that which might be expected
from differences in habitat. (There is consid-
erable difference, of course at the generic and
specific levels.)

(b) Crimea and Caucasus

The warm maritime climate of the Crimea
(Krim) gives an oasis of Mediterranean cli-

FIG. 12. Crimea (Krim); h, d scatter diagram for the pulmonate fauna. Symbols as in Fig. 11.

160 ‘CAIN

FIG. 13. Kuban-Abkhasia; В, d scatter diagram for the pulmonate fauna. Symbols as in Fig. 11. If Poiretia is
considered to be a spiraxid, the symbols at h = 37.5, d = 11.25 and h = 17.5, d = 4.7 should be altered to a

maltese cross.

mate in a highly continental area, with forests
on the hills grading rapidly into dry steppe
country. It has long been known as an outpost
for the Mediterranean fauna, with numerous
endemics.

Fig. 12 gives the h, d distribution for the
Crimea, in which the same bimodality is
shown as before, but the proportion of heli-
cellines has increased greatly to correspond
with drier conditions and the hygromiines
have nearly gone. Large zonitines now ap-
pear. Clausiliids are reduced (compare Fig.
11) but enines are more frequent, and may
well include forms like Zebrina, more ac-
customed to exposure to the sun.

The vastly more extensive and more eco-
logically diversified region of the Caucasus
and Transcaucasia has a rich fauna (and
flora) with numerous endemic species, and
preserves genera and species which have
vanished from Europe, including some snails
now relict in the Caucasus and widespread in
eastern Asia (Likharev & Rammel’meier,
1962). Nevertheless, the snail fauna as a
whole is almost entirely palaearctic in affinity.
The complexity of climate and vegetation in
the Caucasian region requires more than one
diagram. Fig. 13 is for Kuban-Abkhasia, in
Likharev & Rammel'meiers (1962) West
Caucasian district, which has a climate heav-

PALAEARCTIC HELICID SHELLS

C1]
©
= ae

161

FIG. 14. Talysch; в, d scatter diagram for the pulmonate fauna. Symbols as in Fig. 11.

Пу influenced by the Black Sea and rich,
mixed, deciduous forests. Fig. 14 gives the
same information for Talysch, bordering the
Caspian Sea, with a humid subtropical cli-
mate which extends eastwards along the
north Persian coast. Fig. 15 is for Likharev
and Rammel'meier's Armenian district, which
has a highly continental climate with cold
winters and hot dry summers, and consists
mainly of mountainous desert and steppe.
The fauna has affinities with that of Mesopo-
tamia, and the district is classed by them as
part of a Sumerian province. Their detailed
descriptions of the districts and analyses of
their faunas should be consulted. The three

sub-districts illustrated here (out of their eight)
give an epitome of the faunal variation.
Again, the same bimodal distribution is
found as in the previous diagrams. In Kuban-
Abkhasia the upper scatter reaches consider-
ably higher values of h than have been seen
so far, with one large clausiliine and the car-
nivorous oleacinid Poiretia. Large zonitines,
which just appeared in the Crimea, are now a
feature of the lower scatter. Clausiliids are
abundant, including members of the Phae-
dusinae, otherwise eastern Oriental; they do
not, however, take over from clausiliines and
are as scattered as were cochlodinines in the
Carpathians. Large dry-country enines are

162 CAIN

reduced as compared with those in the Cri-
mea. Hygromiines are again abundant and
form most of the middle part of the lower scat-
ter, rather as in the Carpathians but with
larger values of d. Almost the same large
helicines appear as in the Crimea, with the
addition of two endemic species of Caucaso-
tachea. In Talysch (Fig. 14), a reduced ver-
sion of the same picture is seen, with phae-
dusines now a greater part of the upper scat-
ter. Apparently they are specialized for a
rather peculiar climate or vegetation. In the
Armenian district (Fig. 15) the fauna is again
somewhat reduced. Some _ characteristic
hygromiines appear that seem to be adapted
to dry country, and correspondingly the heli-
cellines do not increase. Large zonitines

seem to be absent. The place of Caucaso-
tachea is now taken by two species of Levan-
tina, also helicine, which are strongly hot dry-
country forms. In the upper distribution, there
is a much greater prevalence of enids, and
the clausiliids are reduced to two species of
Armenica (Clausiliinae), a genus confined to
Transcaucasia, Asia Minor and Syria.
Clearly, then, in Figs. 10-15 we have the
same general faunal type, with variations
largely related to variations in climate and
vegetation. The upper limit of the upper scat-
ter varies, as does the extent of filling in of the
upper part (d more than 25 mm) of the lower
scatter. Otherwise the same two scatters ap-
pear, differently filled in, in different districts.
In more forested areas, clausiliids are fre-

FIG. 15. Armenian district; h, d scatter diagram for the pulmonate fauna. Symbols as in Fig. 11.

PALAEARCTIC HELICID SHELLS 163

quent in the upper scatter, hygromiines in the
lower, and, in more open, dryer country, enids
and helicellines take over, except where dry-
country hygromiines take over т the
Armenian district. A closer analysis of climate
and habitats would probably suggest a reason
for this. Throughout the various changes in
the upper parts of each scatter, the faunas of
the lower parts (h or d below 10 mm) remain
remarkably constant, with only a slight in-
crease of pupillines and orculids, and disap-
pearance of the few gastrocoptines, to the
east. Many of these small species are wide-
spread and can find a suitable niche where
large ones might be in difficulty.

The boundary between the Palaearctic and
Oriental regions is notoriously difficult to draw
in the north. In the mountains of Central Asia,
there are a number of endemic hygromiines,
plus others that extend right across to the
mountains or southern coast of Europe
(Likharev & Rammel'meier, 1962, as correct-
ed by Shileyko, 1978a). These mountains
have a harshly continental climatic regime. It
is not surprising, therefore, that the family
Bradybaenidae, with many members accus-
tomed to the rigors of the north Chinese cli-
mate spread into them (Fig. 16, central and

FIG. 1 6. Central Asian mountains (Alai, Transalaiskii; Fergana and Chatkal; Trans-lli range and Semirech'e;
Kirgizian and Talasskii ranges); h, d scatter diagram for the pulmonate fauna. Symbols as in Fig. 11.

164 САМ

FIG. 17. Maritime Territory; h, d scatter diagram for the pulmonate fauna. Symbols as in Fig. 11. If
Isognomostoma subpersonatum is a triodopsine polygyrid, the symbol at h = 4.2, 4 = 6.9 should be altered

accordingly from hygromiine.

eastern ranges). There is an apparent over-
lap, in the lower scatter, of bradybaenids and
hygromiines which may well be reduced if the
central and eastern ranges are considered
separately, or if the species’ detailed habitats
were known. The same might be true of the
few ariophantids. The Eninae now make up
most of the upper scatter (except for those
small and hardy species that extend across
Asia to the Pacific), and clausiliids are miss-
ing.

Near the Pacific Ocean (Fig. 17), the Mari-
time Territory, although with considerable
mixed and deciduous forest, has apparently a
poorer representation than in the Central

Asian mountains. This is especially pro-
nounced in the upper scatter, which is very
poor. Almost the same is true, however, in the
case of the fauna of the cold north-eastern
districts of the U.S.A., which also have an
eastern continental climate with mixed conif-
erous and deciduous woodland.

In these last two diagrams, then, the scat-
ters are maintained (the upper one greatly re-
duced in the Maritime Territory), but by means
of bradybaenids, not helicids (with a few ex-
ceptions) in the lower scatter; bradybaenids
(with a single exception, see Fig. 10) do not
occur in Europe where the helicids are wide-
spread, and take their place in the lower scat-

PALAEARCTIC HELICID SHELLS 165

FIG. 18. European steppe; h, d scatter diagram for the pulmonate fauna. Symbols as in Fig. 11.

ter in the northern Oriental region. Here we
have a replacement of one group by another,
as already shown for very different groups
within the North American fauna, and be-
tween the North American and European
(Cain, 1977a). In the upper scatter, however,
we have only the enhancement of one group
at the expense of another with which it co-
exists over an enormous region; it gives no
grounds for distinguishing the Palaearctic
from the Oriental fauna.

(d) Tundra, steppe and forest

In the diagrams so far, the fauna shown has
contained, from the point of view of snails, a
considerable forest or woodland element,

even in the Armenian and Central Asian re-
gions along water courses. On high moun-
tains in Europe, some woodland forms can
persist in the alpine zones, or sheltered in
crevices and scree, so that montane regions
devoid of woodland can carry woodland spe-
cies. Much of the faunal variation can be
understood as a variation between woodland
in a broad sense, or better, sheltered forms
and open-habitat forms. The change from
helicids to bradybaenids, however, appears to
be due to separate development of faunas
with subsequent meeting, and it is possible
that the replacement of the largely European
helicellines by hygromiines in the Caucasus
and eastwards is so too. Likharev &

166

$
DO К

YL
À LA

CAIN

FIG. 19. Tundra; h, 4 scatter diagram for the pulmonate fauna. Symbols as in Fig. 11.

Rammel'meier's data (1962: 30-32, 36-37),
however, allow one to go further and contrast
such regions with European steppe (Fig. 18)
and with tundra (Fig. 19). In both, as might be
expected, the number of species is reduced
as compared with more forested regions,
most so in the tundra. In the steppe, the few
large molluscs in the lower scatter are almost
all associated with the occurrence of occa-
sional bushes. (Many more species, as
Likharev & Rammel'meier point out, penetrate
along water-courses, but do not belong to the
steppe as such). It is not clear whether their
group of widely ranging species should occur
here as well, but it is unlikely that it should not,

and it has been included in the diagram. The
tundra fauna indeed, apart from the addition
of a few arctic forms, is largely composed of
widely-spread species, of small shell size but
still showing the two scatters. Many of them
appear in the diagrams given here for Europe,
the Crimea and the Caucasus; a few are ab-
sent from Central Asia, and from the Far East.
No species, as Likharev & Rammel'meier
remark, is endemic to the tundra, nor to the
steppe, and only a very few cold-adapted
forms to the tundra plus taiga. (A few in the
taiga belt are Siberian endemics, but with
close relatives in the west.)

Generally speaking, then, at the family and

PALAEARCTIC HELICID SHELLS

FIG. 20. Azores; h, d scatter diagram for the pulmonate fauna. Symbols as in Fig. 11.

subfamily levels, we do not find specialized
faunas, each in a major climatic belt or vege-
tation type. We find instead a single fauna
with a few very tolerant and widespread spe-
cies nearly everywhere, less tolerant ones
coexisting with the widespread ones in more
favourable habitats, and many coming in only
in woodland, or only in open habitats. The
distinction between a woodland faunule and
an open-country faunule is the best to be
found in these regions and, as already indi-
cated, probably accounts for a good deal of
faunal variation from place to place in the
diagrams.

167
(ii) Macaronesia
The Cape Verdes, Canaries, Madeira

group and Azores, like other oceanic islands,
are characterized by much endemism and a
puzzling variation in faunal composition from
one group (or even island) to the next. It is
tempting to ascribe this variation simply to
chance colonization. However, the island
groups, although oceanic, differ considerably
in climate and vegetation (now mostly de-
stroyed), and, until a careful survey has been
made of their different characteristics, it would
be rash to assume that the variation is due to

168 САМ

nothing but chance. One cannot expect the
Azores, formerly covered at lower altitudes by
dense laurel forests and with lower tempera-
tures generally (see Backhuys, 1975, for a
description of their vegetation), to allow the
same species arriving from Europe to survive
as would the hot dry Desertas to the south-
east of Madeira (Cook, Jack & Pettitt, 1972).

Very little seems to have been done on the
Cape Verde fauna. That of Madeira is prob-
ably the richest, and that of the Canaries next
in richness. Backhuys’s excellent volume
gives us an up-to-date picture of the Azores.

The land-snail fauna of Macaronesia, ex-
cluding obviously introduced forms, has only
a single species of Punctum (Endodontidae)

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that is nearctic (Backhuys, 1975: 275), the rest
being all palaearctic. The degree of endem-
ism is high. Two subfamilies of Helicidae, the
Leptaxinae (about 22 species) and Geomitri-
nae (about 65 species) are confined to
Macaronesia, the former in the Madeira
group, Canaries, Cape Verdes, and Azores,
the latter especially well developed in the drier
areas of the Madeira group, except for a very
few which occur in the Azores and one in the
Canaries. In the Helicinae, one genus,
Hemicycla, is confined to the Canaries, with
about 45 nominal species. In the Helicellinae,
the genus Monilearia with about ten species
is also Canarian. The genus Canariella with a
few nominal species (subfamily Helicodonti-

Y
o
o o
de
w
=
we

FIG. 21. Canaries; h, d scatter diagram for the pulmonate fauna. Symbols as in Fig. 11.

PALAEARCTIC HELICID SHELLS 169

nae) is confined to the Canaries. One sub-
genus of Helix consists of a single endemic
species, perhaps still surviving, on Porto
Santo (Madeira). A thin sprinkling of other
helicids, a few of them endemic but most of
them probably introduced, completes the
helicid component, which is therefore very
largely endemic. Even when not restricted to
a single island group, the Macaronesian heli-
cid genera very rarely have species common
to more than one. Such a high degree of
endemism is characteristic of oceanic islands.

No other family except the Enidae has an
endemic subfamily in Macaronesia, but sev-
eral genera or subgenera are confined to it or

x a)
O)

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IAS ”
x ce AR

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пеайу so, and the distribution of several
groups that are also found elsewhere is often
restricted. п the Pupillidae, the genus Leio-
styla, also known from Europe, is widespread
with numerous endemic species (Azores,
Canaries, Madeira). Janulus (Endodontidae)
is remarkable for being known fossil from
Europe, and living in Madeira. There are local
developments of Vitrinidae, Zonitidae (especi-
ally Oxychilus, Azores and Canaries; Retinel-
la (Tyrodiscus), Canaries), Ferussaciidae
(Canaries and Madeira group), Endodontidae
(Discus in Madeira), Clausiliidae (Boettgeria
in Madeira, Balea in the Azores). Perhaps
most conspicuous is the development of the

FIG. 22. Porto Santo, Madeiran Archipelago; h, d scatter diagram for the pulmonate fauna. Symbols as in

Fig: 444

170

CAIN

FIG. 23. Madeira and the Desertas; h, d scatter diagram for the pulmonate fauna. Symbols as in Fig. 11.

endemic genus Napaeus (Enidae, Napaei-
nae), which may or may not merit subfamily
rank, in the Canaries (about 40 nominal spe-
cies) and Azores (7 species) and perhaps
Cape Verdes (one species) but totally absent
from the Madeira group (Wollaston, 1878;
Backhuys, 1975). This genus is known fossil
from Europe; other European fossils have
been ascribed to the Leptaxinae and Geo-
mitrinae, perhaps not very securely. Certainly,
Macaronesia may well preserve a number of
forms that have become extinct in Europe,
more intolerant members of an ecological
group still represented in extreme western
Europe by the lusitanian element of the pul-
monate fauna.

For completeness it should be mentioned
also that the land operculates include one
archaeogastropod (Hydrocena gutta, Azores
and Canaries, nearest relative in Dalmatia),
an endemic subfamily of mesogastropods
(Craspedopomatinae, with about five species
in the Canaries, Madeira group, and Azores,
and nearest relatives in the tropics), and a few
species of the European mesogastropod
Pomatias in the Canaries).

The diagrams (Figs. 20-24) show clearly
the very different composition of the faunas of
each island group, even of the Cape Verdes,
which are poorly known and not recently re-
vised. In the upper scatter, the napaeines of
the Azores and Canaries contrast with the

PALAEARCTIC HELICID SHELLS 171

clausiliids of the Madeira group. In the lower
scatter, the leptaxines of the Azores, Cape
Verdes, and Madeira group are replaced by
the helicine Hemicycla in the Canaries, in
which scatter the lower part is formed by
Monilearia (helicelline), not as in the Madeira
group by geomitrines. In short, we still have
the same two scatters but made up in very
different ways. While the differences in the
lower scatter are not as great as those be-
tween Europe and the Maritime Territory, they
are greater than between many of the other
regions or districts investigated, and those in
the upper scatter are largely the same as be-
tween the clausiliid-rich regions of Europe
and the Caucasus, and the enid-rich Central

Asian mountains, although using a different
subfamily of the Enidae. Nevertheless,
throughout we still get a good approximation
to the same two scatters as are seen in west-
ern Europe and other parts of the world.

DISCUSSION

This investigation shows the maintenance
of a bimodal distribution of h and d among
land stylommatophorans fully retractable into
their shells, from the Macaronesian islands
through Europe and Central Asia to the Mari-
time Territory. Yet, as already indicated for
western Europe as against North America

FIG. 24. Cape Verde Islands; h, d scatter diagram for the pulmonate fauna. Symbols as in Fig. 11.

172 CAIN

(Cain, 1977a), the compositions of the two
scatters can vary remarkably from region to
region. In the present examples, an extreme
case is the replacement of the Helicidae in the
lower scatter by Bradybaenidae in the Central
Asian mountains and the Maritime Territory;
lesser examples are given in the different
ways the lower scatter is made up in different
island groups of Macaronesia. Variation in the
upper scatter in continental regions seems
largely related to difference in available habi-
tats in different regions; it cannot be said yet
that this is not so in Macaronesia. Even in
the apparently straight-forward case of the
helicids and bradybaenids the interpretation is

d
FIG. 25. Bulimulidae; h, d scatter diagram. Symbols as in Fig. 1.

far from simple. At first sight, what has hap-
pened is obvious; during the extremer periods
of the glaciations much of Central Asia must
have been a dry desert with very little life, and
an enormous stretch of country must have
separated the Helicidae in the western Palae-
arctic and the Bradybaenidae in the Far East.
Each family adapted to local conditions (very
successfully, considering the numbers of
species in each) including the same range of
habitats in both. When conditions ameliorated,
each spread out from its refuge areas, to-
gether with the advancing vegetation. There
is now a confrontation of ecologically similar
forms in the central Asian region, but a few

PALAEARCTIC HELICID SHELLS

o°

173

FIG. 26. Streptaxidae; h, d scatter diagram. Symbols as in Fig. 1.

species on either side, no doubt being spe-
cialized in particular ways, are able to invade
new territory, the helicid Zenobiella reaching
the Pacific and Bradybaena fruticum coming
as far west as eastern France. In course of
time there will be further spreading, with elimi-
nation of unfit forms; as most malacologists
refer to the Helicidae as the ‘highest’ evolu-
tionarily of the stylommatophoran snails, no
doubt in the end they will win.

This explanation is plausible but doubtful. In
the first place, the Maritime Territory, although
maritime, has a continental climate, as does
the corresponding area in the New World, the
north-eastern United States and Nova Scotia.

The climate of western Europe is far more
oceanic, and resembles in the northern
hemisphere that of coastal British Columbia,
with the difference that the oceanic influence
spreads inland all over Europe, whereas the
great barrier ranges running north and south
in the western United States and Canada cut
it off abruptly closer to the west coast. There is
a gradient in increasing continentality from
western Europe right across to the Stanovoi
Range, reversing only slightly from there to
the Pacific coast. It is at least as arguable that
the helicid/bradybaenid border is stationary
precisely where each type becomes inferior to
the other. In that case, the present distribution

174 САМ

is а consequence of present ecological condi-
tions, not of past history, and the replacement
in the lower scatter may be as direct a conse-
quence of present-day ecology as is, with
high probability, the replacement in the upper
one.

In the second place, the argument really
assumes that any group, while retaining
its characteristic features, can adapt to any
local ecology possible at all for that general
type of animal and therefore that since
helicid snails occur from the deserts of
northern Africa to the alpine meadows of
Scandinavia, and from the steppes of south-
ern Russia to the extreme Atlantic climate of
Ireland or the Azores, they could equally well
occur in China, if history had allowed. The
helicids are distinguishable from the brady-
baenids chiefly on the genitalia. In the Brady-
baenidae the mucus glands are not long and
branched as in most helicids, and they open
directly or indirectly into the dart-sac, not in-
dependently into the uterus. The physiological
significance of these differences is wholly un-
known.

Many secondary sexual characters—the
shape of the dart in helicids, the shape and
number of the genital chaetae in oligochae-
tes, the various chitinous processes, claspers,
plates, combs and bristle patches in the
genitalia of many insects, the courtship
dances of different species of sticklebacks,
and the courtship songs of many birds, to cite
a few examples—seem to be wholly arbitrary
signals, closely similar in closely related forms
but with one or two different and specific fea-
tures. If they really are signals, not subject to
selection in relation to differences in the spe-
cies’ mode of life, then they may be the best
indicators of phyletic relationship we have
(Cain, in prep.). In that case, they may indeed
be purely historical records in the present ex-
ample; as a matter of history, Europe and the
Far East were separated for a long period by
dry cold desert, and helicids with their peculiar
genitalia developed into their present adap-
tive radiation in the west, bradybaenids in the
east. Had the course of ecological history
been different, we might now have the middle
of the lower scatter made up by helicids and
the outer part of it by bradybaenids (or vice
versa) from the Atlantic to the Sea of Okhotsk.
If the characters of the genitalia are not arbi-
trary, however, and do have some functional
significance other than as signals, the possi-
bility remains that the helicid pattern is adapt-
ed to the milder conditions of the west, the

bradybaenid to the harsher ones of the east.
Remote though this possibility may seem, it
cannot be ignored.

These considerations may apply to the
hygromiine radiation in the Caucasus and
eastward and to the helicelline radiation in
southern Europe, but with the complication
that the helicellines are a polyphyletic group
derived from the hygromiines. Shileyko
(1978b) remarks that the dull-coloured, rather
fragile and often hirsute hygromiines of
Europe are largely forest forms, while the
more solid, less often hirsute, and sometimes
more brightly patterned forms are in dryer
habitats. He points out a characteristic rock-
living facies with more or less flattened and
ribbed shells occurring in Caucasian forms
and probably independently in a European
species. Correspondingly, in coastal regions
of the Mediterranean, with its hot rainless
summers, helicid snails that sit out exposed to
the hot sun (helicellines, sphincterochilines,
and the taxonomically difficult helicine Theba
pisana) have rather solid shells, often very
white and frequently strikingly patterned with
black or yellow bands. Such a facies is clearly
associated with particular habits and may very
well have evolved several times over. Some
helicellines penetrate far into northern
Europe, and one or two have even become
hirsute and hygromiine-like in habits, for
example Xerotricha conspurcata (Germain,
1930), a reversal of the evolutionary trend. If
the special characters of the genitalia are
again phylogenetically rather conservative,
then assemblages of species defined on the
genitalia will be monophyletic, those on other
Characters will not, and the sort of analysis
given by Shileyko (1978b) enables us to trace
out minor or local adaptive radiations.

In our present state of ignorance of the de-
tailed habits of most land-snails, little can be
said of one of the most interesting features of
the family Helicidae, which is its several inde-
pendent excursions into the upper scatter. As
remarked above, several of the helicellines
involved, especially the genus Cochlicella,
live in coastal sand dunes and other maritime
habitats. Here, they do not coincide with
clausiliids and enids, and it is possible that they
are the substitutes in these habitats for the
usual Palaearctic tall-shelled families.

A suggestion for future investigation may
perhaps be made for the high-spired
leptaxine in the Azores, Helixena sanctae-
mariae of Santa Maria. This species was
formerly placed in Napaeus (Enidae) but

PALAEARCTIC HELICID SHELLS 175

Backhuys (1975) showed by dissection that it
is a leptaxine (Helicidae). Of the four species
of Leptaxis in the Azores of which living speci-
mens are known, excluding one certainly in-
troduced, L. azorica azorica occurs on Sao
Miguel, Faial and Flores, L. azorica minor on
Santa Maria, L. caldeirarum on Sao Miguel
(and perhaps Faial), L. drouetiana on Faial,
and L. terceirana on Terceira. (One recently
extinct species, L. vetusta is known from
Santa Maria and one species, L. niphas, only
from the type collection from Sao Miguel). The
present distribution is therefore with a sub-
species of azorica or a related species
(terceirana) on all the large islands except
Sao Jorge, and with a second species on Sao
Miguel (ca/deirarum) and Faial (drouetiana).
Backhuys (1975: 234, 246) reports L. azorica
minor “In more or less primary woods on the
slopes of the mountains (Pico Alto),” and H.
sanctaemariae “in woods along dead leaves,
under logs, under stones, ес.” For Napaeus,
he refers to a forthcoming paper which will
provide ecological data, but his distribution
records show that there are three on Santa
Maria (one of them also in the Canaries, a
rare example of inter-island-group distribution
of a species), four on Sao Miguel and
Terceira, and three on Faial and Flores. It is
just possible, therefore, that H. sanctae-
тапае on Santa Maria is replacing a
napaene rather than a leptaxine ecologically.
Available studies on Cylindrus obtusus
(Fuchs, 1926; Adensamer, 1937; Klemm,
1961; Backhuys, 1969) give no indication of
its mode of life relative to other forms. It is just
possible that it is a high-altitude form com-
plementing the enids; the data given in
Adensamer's paper (1937) do not rule this
out. Nothing seems to be known of the habits
of Discula turricula.

Although the family Helicidae is the most
variable in h, d in the Palaearctic region, it is
much less variable than others elsewhere.
The total scatter for the Bulimulidae is shown
in Fig. 25. This family is most variable in Cen-
tral and South America, its outliers in Melan-
esia and Western Australia being all tall-
shelled. It crosses the bisector much further
than do the helicids. The ecological circum-
stances under which it does so are not known;
but it certainly coincides with the Camaenidae
which occupy much of the lower scatter, and
probably restrict its variation below the bi-
sector. The Bradybaenidae, mainly lower-
scatter, have a number of very tall-shelled

species in China, Korea and Taiwan, and in the
Philippines (Cain, 1978a) occurs a subfamily
of large shells, the Helicostylinae which
ranges from discoidal to tall with no interrup-
tion. Fig. 26 gives the scatter for the carnivo-
rous Streptaxidae, which are equally distrib-
uted in both scatters but do, in general, pre-
serve the gap between the scatters. No analy-
sis of them by faunas has yet been made. The
Camaenidae are of special interest in having
a disjunct distribution. In Central and South
America they coincide with the Bulimulidae
(Fig. 25) and there they occupy entirely the
medium-sized to large-sized shells' area of
the lower scatter—effectively acting like medi-
um to large helicids. In south-east Asia and
northern Australasia, however, they coincide
with a few very tall slender species (Clausilii-
dae, Megaspiridae, Subulinidae) but with no
tall stout ones of other families; they them-
selves fill in the vacant area with the genus
Amphidromus in south-east Asia (Cain, in
prep.) and with various tall shells belonging to
the subfamily Papuininae in the New Guinea
region (Cain, 1978a).

If, then, variation in h, d can itself vary from
family to family, and, within a family, from re-
gion to region according to the others that are
present, it seems likely that the comparative
constancy of the family Helicidae to the mid-
dle and ощег areas of the lower scatter 1$
because it is usually accompanied by a suf-
ficient suite of outer families to fill up the rest
of the two scatters. That there is nothing in-
herent in being a helicid which restricts it is
shown by the occurrence of the various tall-
shelled helicid species. If they had not been
there, presumably helicids could have filled
the whole range, as the streptaxids do. But if
this is $0, presumably the enids, or clausiliids
could equally have done so, given the ecolog-
ical opportunity. How, then, did these families
come together in the first place and share out
the ecological opportunities in the way we see
now?

ACKNOWLEDGMENTS

| am grateful to Dr. G. M. Davis and Dr. R.
Robertson for criticism of this paper. | thank
most especially H. Wallace and Carol Roberts
of Philadelphia, without whose delightful and
discriminating hospitality | could not have
done much of the work for it.

176 САМ

LITERATURE CITED

ADENSAMER, W., 1937, Cylindrus obtusus
(Draparnaud, 1805), seine relikthafte Verbreitung
und geringe Variabilität, sowie zoogeo-
graphische-phylogenetische Betrachtungen über
alpine Mollusken überhaupt. Archiv für
Molluskenkunde, 69: 66-114, pl. 4.

BACKHUYS, W., 1969, The elevation effect in
Cylindrus obtusus (Draparnaud 1805). [Ab-
stract.] Malacologia, 9: 251-252.

BACKHUYS, W., 1975, Zoogeography and tax-
onomy of the land and freshwater molluscs of
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MALACOLOGIA, 1981, 21(1-2): 177-208

CLINES, CONVERGENCE AND CHARACTER DISPLACEMENT IN NEW
CALEDONIAN DIPLOMMATINIDS (LAND PROSOBRANCHS)

Simon Tillier

Laboratoire de Biologie des Invertébrés marins et de Malacologie, Muséum national
d'Histoire naturelle, 55, rue Buffon, F-75005 Paris, France

ABSTRACT

Eleven diplommatinid species, seven of them previously undescribed, are found in New
Caledonia and adjacent islands. Two species are endemic to the adjacent islands, and the nine
New Caledonian mainland species show varying degrees of endemism. Up to three species
were found to be sympatric. These diplommatinids occur from 0 to 1000 m in elevation, in very
dry to very wet environments. All the species live in more or less decomposed leaf litter.

Species vary considerably in both shell size and shape, and form a continuum of shell char-
acters. In many cases the species can be distinguished only by their anatomy. Except in cases of
species interaction, shell shape is correlated with moisture. Species exhibit clinal variation in
shell characters that are related to environmental conditions. Shell characters overlap when
species are allopatric, and diverge when sympatric. This type of character displacement is so
common that the clinal variation could be interpreted to be the result of species interaction on a
large scale.

The female genital apparatus exhibits four evolutionary steps in a process which may be either
the acquisition or the loss of a seminal receptacle. This process probably occurred many times in
the diplommatinid stock. Added to this the probable convergence of shell characters makes the

value of supraspecific names dubious.

INTRODUCTION

The original purpose of this study was to
discriminate among and accurately describe
the New Caledonian species of the family
Diplommatinidae, which were poorly known
from only a few samples of shells collected at
the end of the last century. Sorting out the
species of these very small land proso-
branchs, one to four millimeters high, was in
fact very difficult. It is always easy to distin-
guish several species when they occur to-
gether and in a small number of samples.
However, the more than one thousand shells
collected in fifty-six New Caledonian localities
form nearly a continuum in shell characters. It
became obvious that the shell characters
used for discriminating species since Kobelt’s
revision (1902) are inadequate to describe
species and supraspecific groups. This study
attempts only to address the problems at the
specific level. The problems at the generic
and suprageneric level, in particular the defi-
nition of genera and the history of the group
from a biogeographical point of view, cannot
be solved without much more data. Accord-
ingly, supraspecific levels will be treated only
superficially.

This study is based on two main ideas: 1)

the female genital anatomy is less variable
than other characters, and allows one to
recognize to which species an animal be-
longs; all other characters can be convergent;
2) Peake’s observation (1973) that sympatric
species do not overlap morphologically
proved particularly useful and stimulated my
search for character displacement and analy-
ses of clines.

Diplommatinid distribution and nomenclature

Since Tielecke (1940) established his clas-
sification of the superfamily Cyclophoracea,
the family Diplommatinidae (= Тееске’$
Cochlostomatidae: Solem, 1959) is divided
into two subfamilies: the Cochlostomatinae of
Europe and the Diplommatininae, which are
mainly east Asian and possibly include the
doubtfully attributed South American Adelo-
poma. In the western Pacific region, the
Diplommatininae occur in Japan, the Mari-
anas, Caroline, Palau, Bismarck, Solomon,
Fiji, Samoa and Tonga islands, and reach
Norfolk and Lord Howe islands and eastern
Australia (Solem, 1959: fig. 17). Most genera
are relatively well defined on the basis of their
shell characters, but this is not the case in the
Diplommatina-Palaina group to which all the

(177)

178

southern species belong, including the New
Caledonian ones. Rensch (1929) and Van
Benthem Jutting (1948) considered that the
presence of an apertural tooth characterizes
Diplommatina, but the study of some Solo-
mon Island species (Solem, 1960b; Tillier,
unpublished) and of New Caledonian species
(this study) shows the insignificance of this
character in taxonomy, even at the specific
level. Although Peake (1973) relegated Solo-
mon islands species to Diplommatina,
Palaina is used here for New Caledonian
species (as was done by Solem (1959) for
New Hebridean ones) for the sole reason that
the type-species of Ра/ата is found to be
geographically much closer to New Caledonia
than the type-species of Diplommatina. This
choice is arbitrary and does not allow any
conclusions about relationships within the
group. At least Palaina macgillivrayi, which
is the type-species from Lord Howe Island,
does not seem incompatible in any character
with New Caledonian species with reference
to the generic level (Figs. 1, 2).

Kobelt & Moellendorff (1898) and Iredale
(1937, 1944, 1945) used shell shape as a
supraspecific character within Palaina
(names listed by Solem, 1959). This study
shows that this character cannot be consid-
ered diagnostic before all data concerning the
variability of the species have been compiled.
As comprehensive data are not available for
most species, no subgeneric groupings are
used here.

Habitat and dispersal

All New Caledonian species are in the leaf
mould during the day. They are almost always
found at ground level. In only one of the fifty-
six collecting localities were they found in
humus accumulated at the bases of Pand-
anus leaves. The wetter the environment is,
the more they are dispersed in the litter. When
the environment dries they tend to concen-
trate where humus retains moisture, i.e., in
decaying wood interstices or in a very small
wetter surface of the litter. This pattern prob-
ably explains why the most important samples
here studied were collected in relatively dry
conditions. This need for wet humus may ex-
plain why the snails are mostly found in forest,
but occasionally they are found in maquis,
particularly in the northernmost part of New
Caledonia, where the latter provides sufficient
plant cover. When several species are found
together, field observations do not show any

TILLIER

ЕЕ: e
Howe Island, 820m, AMS-C 191369. A and В,
shell; C and D, operculum; E and F, female genital-
ia. Scale line, A and B, 2.5mm, C, D, E and F,
1.25 mm. BC, bursa copulatrix; O, oviduct; U, uter-

Palaina macgillivrayi, Mt. Gower, Lord

Us.

А =

м 12 и с

FIG. 2. Radula of Palaina macgillivrayi, same ani-
mal as Fig. 1. Scale line 0.025 mm.

kind of specialization. Although no accurate
test was made, it seems that sampling in a
very small surface (+400 ст?) in a wet en-
vironment gives the same proportions of spe-
cies as sampling in a larger surface (i.e., a few
square meters). In fact, ecological differences
among species have been detected only by
Statistical analyses of environmental variables
at each station.

Data concerning the collecting stations are
given in Table 1 and Fig. 7. One sees that
Palaina was not collected in Ouvéa and Lifou.
It is possible that we failed to collect them, but
it is also possible that Pa/aina has not yet col-

NEW CALEDONIAN DIPLOMMATINIDS 19

onized them; these two islands are the most
recent in the New Caledonian archipelago.
On the mainland no Ра/ата was collected
higher than 1000 m, and we have collected
enough at such altitudes to interpret the ab-
sence of Ра/ата as significant. The high alti-
tude stations are wetter and colder than those
supporting Palaina, but it may also be re-
marked that in New Caledonian high altitude
rainforest, vegetation decays much more
slowly than elsewhere. As a result there is an
absence of real humus which could be a limit-
ing factor for Palaina.

Peake (1968, 1969, 1973) postulated that
passive transport was the most important fac-
tor in the dispersal of small land snails such
as diplommatinids, even within terrestrial
areas. If it is true that no other type of trans-
port can be postulated for the colonization of
isolated islands such as the Loyalty Islands,
this is not the case for colonization inside the
mainland of New Caledonia and possibly for
the closest islands (Belep Islands, Isle of
Pines) which were probably not permanently
isolated by the sea. As a matter of fact, the
occurrence of clines over small distances is
an argument for the predominance of active
dispersal. For example, in cases where we
observe a cline along a steep slope over a
short distance (e.g., Palaina boucheti in the
Paeoua), the predominance of passive trans-
port down the slope would imply that the vari-
ability observed at the summit influences the
variability at the bottom. This is not the case in
any such cline that we have observed; on the
contrary, the few aberrations observed (e.g.,
Palaina mariei on the Paéoua) consist in the
presence of the low altitude form also at the
summit. This suggests that the dispersal is
active, and we have no reason to presume
that Palaina spreads inside each island by
other major means (small mammals are ab-
sent and birds scarce).

Radula and feeding

| have not found any specific differences
between New Caledonian Palaina radulae. All
are taenioglossate with similar teeth (Fig. 3).
The central tooth has generally five cusps, the
first lateral four, the second lateral three or
four, and the marginal teeth have two or three;
the minor variations in number of cusps are
caused by their partial or total fusion. As indi-
cated by Peake (1973), the Ра/ата species
are probably grazers. It is quite surprising to
observe that the size of the teeth and their

œ
=
eS

FIG. 3. Radulae of New Caledonian Palaina. A, Р.
montrouzieri, Lindéralique (sta. 11). B, P. perro-
quini, Mt. Guemba (sta. 47). C, P. mariei, Me
Maoya (sta. 28). D, P. nanodes, Touaourou (sta.
48). Scale line 0.025 mm.

Cusps vary much less than the size of the
animals (Fig. 3). The central tooth is always
about the same size in all species and the
greatest differences in size are found in the
marginal teeth. However, the size of the latter
varies only in the ratio 1:2 as the shell height
varies in the ratio 1:4. When compared with
the very large differences in the size of the
animals, this radula similarity suggests that
animal size is not related with food as sug-
gested by Peake (1973). The niches of the
sympatric species are therefore probably not
differentiated by the particle size of the food,
for which competition possibly occurs.

Shell and operculum

All New Caledonian, Australian and some
of the Solomon Islands species of Palaina
have similar opercula. They are thin, corne-
ous, slightly concave and oligogyrous (Fig. 4;
Tillier, unpublished). The opercula of these
species have an arcuate, narrow thickening,
parallel to the columellar border; they are at-
tached to the foot by their central area, which
is granulous. In some Solomon Islands and
Lord Howe Island species, the operculum is
more developed and is fixed to the foot by a
lamellar process, protruding internally, and

180 TILLIER

FIG. 4. Operculum of P. mariei, Mé Maoya (sta. 28).
Scale line 0.125 mm.

parallel to the columellar side of the aperture
(Fig. 1c, d). The thickening of New Caledon-
ian opercula is probably homologous to this
process.

Shell shape varies from a high and conical
morphotype, called Macropalaina as a genus
by Moellendorff (1897), to a short and stout
one which may be called Ра/ата, or even
Cylindropalaina when the shell approaches a
perfect cylinder in shape. All intermediates
occur and could be called the Velepalaina
morphotype. Each species has a definite
range of morphotype variability, either from
Macropalaina to Velepalaina and Palaina or
from Velepalaina to Palaina and Cylindro-
palaina. None of these names can have tax-
onomic value until each type-species has
proved to represent a distinct group of spe-
cies within the Diplommatina-Palaina com-
plex. It will be demonstrated further that the
variations of the morphotypes are correlated
with environmental conditions, and in particu-
lar with moisture. Comparisons with morpho-
types found in other Melanesian regions may
be interesting. The Ve/epalaina morphotype is
found in eastern Australia and in the New
Hebrides (Iredale, 1937; Solem, 1959). In
Australia, Eclogarinia represents a morpho-
type characterized by a high conical shell with
the penultimate whorl narrower in diameter
than the preceding one. “Eclogarinia” gowl-
landi does not exhibit any other peculiar ana-
tomical or morphological feature (Tillier, un-
published). This morphotype is quite common
farther north and is found also in New Guinea.
In the Solomon Islands shell shapes vary be-
tween this type and typical Palaina, with inter-
mediates quite similar to the stoutest shells of
the New Caledonian Palaina perroquini (Fig.
29A; Peake, 1973, Fig. 1). Lord Howe Island
species vary around the typical Palaina
morphotype (the type-species among them!),

whereas the two Norfolk Island species have
a loose last whorl but otherwise approach the
Velapalaina morphotype (Iredale, 1945). Sin-
istral species are dominant in Australia and
the Solomon Islands, and no dextral species
is found in New Caledonia, New Hebrides,
Norfolk and Lord Howe Islands.

All New Caledonian species have thin
shells, with an ornamentation consisting of
very thin spiral threads crossed by radial
lamellae, which may project as wings in well-
preserved juvenile specimens of some spe-
cies. The distances between ornamental ele-
ments on each whorl vary but tend to be dif-
ferent in each species. In well-preserved spe-
cimens it can be observed that the spiral
threads are continuous over the radial lamel-
lae. Just before the adult aperture is formed
there is no significant change in the interval
between successive radial ribs. A first peri-
stome is formed by the expansion of one rib,
and then the ribs are very close and not ex-
panded on a very short distance before the
definitive expanded peristome is formed (Fig.
26). In all species but one, the peristome is
approximately parallel to the shell axis.

This type of ornamentation and aperture is
the commonest in Melanesia, but all Solomon
Islands species and some Lord Howe Island
species have a thicker shell and a different
type of aperture. In these species, the radial
ribs become closer about one quarter of a
whorl before the peristome is formed; the lat-
ter is very thick and formed by crowded,
slightly expanded radial ribs (see Rensch,
1929, fig. 6 and Palaina macgillivrayi, Fig.
1b).

The embryonic shell is irregularly pitted in
the same way in all New Caledonian species,
and is similar in other Melanesian species ex-
amined.

Animal and general anatomy

A preserved animal is shown in Fig. 5. The
most striking feature is the well-defined pro-
podium, mesopodium and metapodium,
which are separated by distinct and constant
grooves. This feature, which is exceptional in
marine mesogastropods (Fretter & Graham,
1962), may also be seen in the Cochlosto-
matinae. According to Girardi’s figures
(1978), such grooves are absent in poteriids.
This character could serve to define families,
but unfortunately | could not check it in other
Cyclophoracea and cannot reach any defini-
tive conclusion. Among other land proso-

NEW CALEDONIAN DIPLOMMATINIDS 181

FIG. 5. Animal of P. montrouzieri, Pombei (sta. 13).
Scale line 0.5 mm. MC, mantle cavity; OP, opercu-
lum; R, rectum; U, uterus.

branchs, pedal grooves are found also in
truncatellids (Fretter & Graham, 1978).

The mouth opens into a slit between two
well-defined, rounded lobes. Above these
lobes the head forms a sort of apron, posteri-
orly limited by the anterior pedal groove which
separates the propodium from the meso-
podium. The animals are completely white,
except the tentacles that are sometimes grey.
There is always a grey spot at the base of the
tentacles, in front of the eyes. This spot may
be either rounded (Fig. 5) or form a transverse
bar joining the eye; its shape is neither spe-
cific nor sex-determined, although each indi-
vidual shows one or the other of the two spot
shapes.

The mantle cavity occupies about the last
one and a half whorls of the visceral mass
(Fig. 6). The uterus or prostate runs along the
columellar side of the mantle cavity, without
protruding into the upper visceral cavity, and
is bordered externally by the rectum. The kid-
ney occupies about one quarter of a whorl
above the upper part of the mantle cavity and
hides the small heart that lies just under its
proximate extremity. The oesophagus runs up
along the columella before bending back out-
wards into a large cylindrical stomach, about
one third of a whorl long. The stomach has no
distal caecum but a distal inflated ring, which
is probably the equivalent, whereas the
Cochlostomatinae have a true caecum. Fecal
pellets are formed in the proximal intestine
which is parallel to the spire, less than half a

whorl long and often regularly inflated by fecal
matter. In the distal intestine the pellets are
always well formed and distinct. Just proxi-
mally to the mantle cavity, the intestine forms
one loop before running into the latter be-
tween the pallial gonoduct and the kidney.
The same disposition is found in the Coch-
lostomatinae. Among Cyclophoracea poteri-
ids have the same type of stomach but with-
out any trace of a caecum (Girardi, in /itt.; data
lacking for other families).

Genital anatomy, reproduction and growth

Males have no penis, and thus males and
females have the same disposition of their
genital apparatus. The gonad lies along the
columellar side of the visceral mass for about
one whorl, starting from the beginning of the
third whorl from the apex. The genital duct
then coils along the columella, together with
the oesophagus, to the upper parietal corner
of the mantle cavity aperture where it opens
just beside the anus (Figs. 5, 6). At the prox-
imal end of the mantle cavity it enlarges

FIG. 6. General anatomy of P. mariei, Ме Maoya
(sta. 28). Scale line 0.5 mm. The upper intestine is
inflated by a pellet. BC, bursa copulatrix; G, gonad;
|, intestine; К, kidney; О, oviduct; OE, oesophagus
(sectioned); OP, operculum; R, rectum; ST, stom-
ach; U, uterus.

182 TILLIER

abruptly into a prostate or a uterus. In males
there is no other morphological differentiation,
but in females the differentiation of the distal
oviduct, just proximally to the upper extremity
of the uterus, into a bursa copulatrix and a
seminal receptacle provides the only specific
anatomical characters that | could find in
Palaina. These female organs are located
behind the intestinal loop (Fig. 6).

The bursa copulatrix is relatively constant in
shape and disposition within each species. Its
inflated head is generally appressed against
the proximal end of the uterus, but its stalk
may point either upwards or downwards from
the distal oviduct; in the latter case its head
may occasionally, but constantly within a
population, point within the intestinal loop in-
stead of above it.

The seminal receptacle may be absent or
present, as in the Cochlostomatinae (Giusti,
1971). Four steps in its position and develop-
ment are found: 1) The seminal receptacle is
well developed and opens into the oviduct
close to the base of the stalk of the bursa
copulatrix: found in New Caledonian Palaina
montrouzieri (Fig. 20); 2) The seminal re-
ceptacle is well developed, but opens into the
basis of the bursa stalk: found in some
Solomon Islands species (Tillier, unpub-
lished); 3) The seminal receptacle is reduced
to a swelling located approximately in the
middle of the bursa stalk, on the outside of the
bend of the latter: found in New Caledonian
Palaina mariei (Fig. 22), P. obesa (Fig. 23),
and in some Solomon Island species (Tillier,
unpublished); 4) The seminal receptacle is
absent in New Caledonian Ра/ата mareana
(Fig. 34), P. perroquini, P. boucheti (Fig. 25),
P. opaoana (Fig. 32) and P. nanodes (Fig.
27), and in some Australian, Solomon Islands
(Tillier, unpublished) and Lord Howe species
(Figs 1).

Only the two extreme arrangements are
known in the Cochlostomatinae (Giusti,
1971), and an arrangement somewhat equiva-
lent to the intermediate ones is found in the
Pupinidae (Tielecke, 1940) where it is there-
fore not a familial character.

We have no data on reproductive behavi-
our, and do not know how individuals recog-
nize each other, the males having no penis.
The populations collected are formed of sets
of specimens of the same apparent age, and
it therefore seems that all individuals of one
population reproduce at the same time.

Berry (1963a, b) observed that the space
between two radial ribs represents one day’s

growth in Malayan Opisthostoma. As far as
this result can be generalized for any Diplom-
matininae, this means that species with dis-
tant varices grow faster than species with
close varices. If this hypothesis is true, the
time necessary before New Caledonian spe-
cies begin to build their peristome varies from
about 80 days in Palaina mareana to about
160 days in P. nissidiophila. The genital ap-
paratus is formed at about the same time as
the first expansion of the peristome, but
reaches its full development only when the
second expansion is built.

SPECIES VARIATIONS AND
INTERACTIONS

Schindel & Gould (1977) reviewed and dis-
cussed character displacement, with particu-
lar reference to land snails. The methodology
herein adopted for demonstrating character
displacement is very simple, and consists of:
1) An analysis of the relationships between
the variations of the species and the varia-
tions of their environment; 2) An analysis of
the variations found in populations of sympat-
ric species, with reference to the first analysis.
| cannot but hope that these analyses provide
a rebuttal to Schindel & Gould’s statement ac-
cording to which the fossil record is superior
to the living one for assessing such evolution-
ary processes.

Materials and methods

More than 1000 specimens, collected at 56
stations all over New Caledonia and adjacent
islands, were used for this study. Shells are
much more numerous than animals taken
alive, but living animals were found at 33 sta-
tions. Two samples were borrowed from the
National Museum of New Zealand (NMNZ),
Wellington; all the other specimens are
housed in the Muséum national d'Histoire
naturelle, Paris (MNHN), and consist of: 1) A
few old samples, collected mainly by Marie
around Nouméa and the Baie de Prony (=
Baie du Sud), which are important because
they contain most of the previously described
type-specimens; 2) About nine-tenths of all
the material was collected by Philippe
Bouchet between April 1978 and July 1979,
and by Bouchet and Tillier in June—July 1979.

A complete list of the stations is given in
Table 1, and their localities are shown in Fig.

NEW CALEDONIAN DIPLOMMATINIDS 183

7. For each station we know the altitude, the
type of vegetation and the rainfall. The latter
was estimated from Moniod's data (1966)
published by ORSTOM. In some cases the
value given by the ORSTOM map is aber-
rant. For example, the northwestern moun-
tains, the summits of which are covered with
high altitude rainforest, are in a very dry zone
of the map. In such cases | estimated the rain-
fall as being the same as in another place with
the same vegetation where it has been meas-
ured.

The number of specimens at each station
will be found in brackets within the list of ma-
terial of each species in the systematic part of
this work. Shell height, H, and shell diameter,
D, were measured on 937 shells (in one sam-
ple of more than 200 shells, only 128 were
measured to avoid a disproportionate influ-
ence on the results of the analyses). For
measurements, shells were placed under the
microscope with the aperture upward and
dimensions measured on mm paper placed
under the camera lucida; precision was
+10 um. H is the largest dimension parallel to
the shell axis, D is the diameter of the body
whorl, perpendicular to the shell axis, from the
outer border of the aperture to the most ex-
ternal opposite point of the body whorl. The
number of radial ribs should be useful for cline
analyses. It was not used because of the im-
possibility of obtaining reliable counts without
counting all the ribs of one shell, which is im-
practical with such a large number of small
shells.

After shells were measured, most of the
preserved specimens were dissected. This
was useful for establishing anatomical varia-
bility of each species and absolutely neces-
sary for naming the specimens representative
of the morphological overlap of two species.

Statistical methods

The statistical analysis was made to try to
understand the relations, within different sets
of specimens, between the dimensions and
shape of the shells, and the environmental
variables. The IRIS 80 computer of the Uni-
versite Pierre et Marie Curie, Paris, was used
to perform: 1) The analysis of the distribution
of the variables with the HISTO program; 2)
The factor analysis of several sets of speci-
mens for several sets of variables with the
ANACOR program. Both programs come
from the statistical library of the computer and

were published by Jambu & Lebeaux, 1979
(HISTO) and Benzécri, 1980 (ANACOR).

All data were first computed in a single
matrix with one row for each specimen, num-
bered from 1 to 937. In each row the charac-
teristics of each specimen are written in nine
columns. These variables are the species,
coded by a number between 1 and 11, shell
height H, shell diameter D, number of the sta-
tion between 1 and 56, longitude, latitude and
rainfall. Two additional morphometric data,
which in fact were more significant than height
and diameter, were calculated for each speci-
men and introduced as columns. These are
shell size, approximated by the product H x
D, and shell shape, approximated by the ratio
H/D. The sets of specimens (all specimens
from one locality, or all specimens belonging
to one species, etc.) and different sets of vari-
ables for these specimens were extracted
from this general table for the analyses.

The HISTO program then permitted estab-
lishing histograms for each quantitative vari-
able, partitioned into twenty classes of equal
amplitude. These histograms do not show any
Classic distribution (normal, y, etc.) for any
variable, even after simple transformations
and even when established species by spe-
cies and population by population. For this
reason | turned to factor analysis (corre-
spondence analysis), which may be used
without any preliminary hypothesis about the
distribution of the variables. As correspond-
ence analysis requires nearly equal fre-
quencies of the classes, the basic histograms
were used previous to each analysis to estab-
lish class limits allowing subequal effectives
of classes. As a result the same symbols do
not represent the same absolute values in the
different analyses.

Once the variables have been grouped into
modalities of equal effectives, the ANACOR
program analyses the matrix coded 0 or 1. It
locates each individual in the space of the
variables (or each modality in the space of the
individuals) and extracts the principal com-
ponent axes, classified in function of the per-
centage of variance loading on them. The
final result is a projection of the individuals
and of the variables on the planes determined
by the axes of the principal components. Only
the projections of the variables are repro-
duced here. The projections of the individuals
were used to check the verisimilitude of pro-
posed interpretations, but are unreproductable
in a printed paper (937 numbered points on
each).

184 TILLIER

TABLE 1. List of collecting stations.

1. Pott (Веер Islands), bay of Panane, thalweg with Gaiacs. Rainfall 1190 mm. Bouchet and Chérel coll.
27.8.1978. 2. Ап (Веер Islands), bay of Pairome, littoral dry forest with Cycas on sand and pumice. Rainfall
1190 mm. Bouchet and Chérel coll. 25.8.1978. 3. Мепапе (Daos du Nord Islands), northeastern bay, littoral
dry forest on sand and pumice. Rainfall 1190 mm. Bouchet and Chérel coll. 23.8.1978. 4. Mt. Tiébaghi,
500 т, low maquis on peridotite. Rainfall 1200 mm. Tillier coll. 6.1979. 5. Le Cresson, 100 т, dry forest on
calcareous outcrop. Rainfall 1200 mm. Tillier coll. 30.6.1979. 6. Koum, 80 т, dry forest on calcareous
outcrop. Rainfall 1200 mm. Tillier coll. 30.6.1979. 7. Mandjélia, 400 m, 5 km from the sawmill, rainforest.
Rainfall 1900 mm. Tillier coll. 2.7.1979. 8. Oubatche, 500 m, rainforest. Rainfall 2500 mm. Hedley coll.
(AMS). 9. Ruisseau de l'Etoile du Nord (Oué Paoulou), 150 m, dry forest probably on a calcareous outcrop.
Rainfall 1100 mm. Tillier coll. 30.6.1979. 10. Kavatche, 50 m, river drift in slightly disturbed rainforest.
Rainfall 2200 mm. Bouchet coll. 25.11.1979. 11. Lindéralique, 20 m, decaying plant accumulation in holes in
a massive calcareous outcrop. Rainfall 2267 mm. Bouchet coll. 26.11.1978. 12. Taom Mt., 900 m, altitude
rainforest in a thalweg, on peridotite. Rainfall 2500 mm. Tillier coll. 3.7.1979. 13. Pombei, 100 m, rainforest.
Rainfall 2781 mm. Bouchet and Tillier coll. 7.1979. 14. Momies de la Faténaoué, 150 т, dry forest, Rainfall
1250 mm. Tillier coll. 4.7.1979. 15. Poindimié, 20-50 т, rainforest 300 т from the shore. Rainfall 3200 mm.
Bouchet coll. 29.9.1978. 16. Plateau de Tango, track to Bobeitio, 300-350 т, rainforest. Rainfall 1800 mm.
Bouchet coll. 24.12.1978. 17. Aoupinié, 350 т, track to the saw-mill above Goa tribe, rainforest. Rainfall
2500 mm. Bouchet coll. 18. Сорт, 50 m, southwestern lower slopes of the Mt. Aoupinie, rainforest. Rainfall
1525 mm. Bouchet coll. 6.5.1979. 19. Forêt Plate, 540 m, slope of Mt. Paéoua, rainforest. Rainfall 1841 mm.
Bouchet and Tillier coll. 15.7.1979. 20. Mt. Paéoua, 950-1000 т altitude rainforest. Rainfall 3000 mm. Tillier
coll. 5.7.1979. 21. between Nékliai and Nétéa, 100 т, lower slopes of Mt. Boulinda, rainforest. Rainfall
1500 mm. Tillier coll. 7.7.1979. 22. Nindiah, 50 m, near the mission, small calcareous outcrop. Rainfall
1842 mm. Bouchet coll. 30.12.1978. 23. Plaine aux Gaiacs, probably sublittoral dry forest. Rainfall
1000 mm. Dell coll. (NMNZ). 24. Népoui, Presqu'île de Muéo, littoral dry forest. Rainfall 1000 mm. Tillier coll.
5.7.1979. 25. Adio caves, 180 m, decaying plant accumulation in holes in calcareous outcrop. Bouchet coll.
6.5.1979. 26. Col des Roussettes-Bogui, 150 m, rainforest. Rainfall 1600 mm. Bouchet coll. 15.5.1978. 27.
Col des Roussettes, 550 m, rainforest. Rainfall 1658 mm. Kuscher coll. 31.10.1978 (NMNZ). 28. Junction of
the two rivers running down the Mt. Mé Maoya and the Dent de Poya, 50 m, rainforest. Rainfall 2000 mm.
Bouchet and Tillier coll. 15.6.1979. 29. Mt. Me Ori, 530 m, southeastern slope, rainforest. Rainfall 2000 mm.
Bouchet coll. 30.4.1979. 30. Col de Petchekara-Dothio, 250 m, rainforest. Rainfall 2000 mm. Bouchet coll.
8.7.1978. 31. Oua Oué, 50m, decaying plant accumulation in holes in calcareous outcrop. Rainfall
1364 mm. Bouchet coll. 31.12.1978. 32. Рое beach, secondary dry forest on sand. Rainfall 1000 mm.
Bouchet coll. 19.8.1978. 33. Roche Percée, Bourail, littoral maquis on sand. Rainfall 1000 mm. Bouchet coll.
10.12.1978. 34. Col. des Arabes, 100 m, maquis. Rainfall 1000 mm. Bouchet, Tillier and Waren coll.
9.6.1979. 35. Nassirah, 100 m, on the right slope of the Fonwhary valley, rainforest. Rainfall 1300 mm
Bouchet coll. 8.7.1978. 36. Mine Galliéni, 700-750 m, gallery forest in a thalweg on peridotite. Rainfall
1600 mm. Bouchet coll. 19.5.1979. 37. Mt. Dzumac, 1000 m, altitude rainforest. Rainfall 3000 mm. Bouchet
and Tillier coll. 6.1979. 38. Plaine aux Cailloux, 100 m, rainforest. Rainfall 1267 mm. Bouchet coll. 3.2.1979.
39. Ndé, 60 m, hill near the tribe, secondary forest. Rainfall 1267 mm. Bouchet coll. 2.7.1978. 40. Yahoue,
200 m, slopes of the Mt. Koghi, rainforest. Rainfall 1400 mm. Bouchet coll. 24.11.1978. 41. Nouméa, old
collections, probably dry forest. Rainfall 1100 mm. 42. Baie Tina, Nouméa, littoral dry forest. Rainfall
1200 mm. Bouchet coll. 16.12.1978. 43. Riviere Bleue, 150 m, rainforest on peridotite. Rainfall 3000 mm.
Bouchet coll. 6.1.1979. 44. Mamié, 50 т, high maquis with boulders on peridotite. Rainfall 2800 mm.
Bouchet coll. 14.1.1979. 45. Waho, 20 т, rainforest on uplifted coral reef. Rainfall 2800 тт. 46. Mt.
Guemba, 200 m, rainforest on peridotite. Rainfall 2938 mm. Bouchet coll. 13.1.1979. 47. Mt. Guemba,
450 m, rainforest on peridotite. Rainfall 3200 mm. Bouchet coll. 16.2.1979. 48. Touaourou, 10 m, rainforest
on uplifted coral reef. Rainfall 3000 mm. Bouchet coll. 8.12.1978. 49. Kuebeni, 50-80 m, rainforest on slope
on peridotite, left bank of the Kuébéni river. Rainfall 2500 mm. Bouchet coll. 15.2.1979. 50. Goro, 15 m,
rainforest on peridotite. Rainfall 1900 mm. Bouchet and Chérel coll. 8.4.1979. 51. Baie de Prony, on perido-
tite, old collections. Rainfall 2800 mm. 52. Mt. Оипдопе, 450 т, rainforest on steep slope. Rainfall 3500 mm.
Bouchet coll. 1.10.1978. 53. Ouro, Isle of Pines, 15 m, littoral dry forest on uplifted coral reef. Rainfall
1800 mm. Bouchet coll. 21.10.1978. 54. Enéné, Mare Island, 60 m, wet bottom of a large dolina. Rainfall
1500 mm. Bouchet coll. 7.4.1979. 55. Меди, Mare Island, dry forest on uplifted coral reef. Rainfall 1500 mm.
Bouchet coll. 4.1979. 56. Nece, Mare Island, 15-20 m, dry forest on uplifted coral reef. Rainfall 1500 mm.
Bouchet coll. 5.4.1979.

NEW CALEDONIAN DIPLOMMATINIDS 185

FIG. 7. Map of the collecting localities (listed in Table 1).

Geography, ecology and morphometric
variability

Each species exhibits a well defined range
for each geographical, ecological and morph-
ometric variable. The specific ranges for
height, diameter, size, shape and rainfall are
given in Figs. 8 to 11. The geographic data
are summarized in Table 2. Altitude was elim-
inated from this step onwards because its
significance, if it has any, is masked by the
influence of rainfall; nearly all the eastern
coast is very wet from sea level to high alti-
tudes and the rainfall is approximately propor-
tional to the altitude along the western coast.
All the intermediate situations are found when
crossing New Caledonia.

Palaina mariei is the only species that may
be expected anywhere on the mainland, ex-
cept in the extreme north. It is also the only
species that exists in the whole rainfall range

of New Caledonian Palaina, from 1000 to
3500 mm a year. It is a rather small species of
variable shape, but occupies the mid-range of
all shapes. It has been found sympatric with
Palaina montrouzieri, P. opaoana and Р.
boucheti.

Palaina montrouzieri and P. opaoana have
about the same mid-size, but the former may
attain larger sizes than the latter. They are
found in the same rainfall range of 1000 to
3125 mm rain a year but occupy adjacent
geographic ranges, P. montrouzieri being
found in northern, central, eastern and possi-
bly southern New Caledonia, and P. opaoana
being found only in central New Caledonia but
very commonly along the western coast.
Palaina montrouzieri generally has a more
elongate shape than P. opaoana.

Palaina boucheti is a small species, gener-
ally less elongated than P. mariei, occurring
throughout southern, central, eastern and

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NEW CALEDONIAN DIPLOMMATINIDS 187

boucheti

0.6 1

perroquini

kuniorum

montrouzieri

1.5 2 D

FIG. 8. Scatter diagram of New Caledonian species of Palaina for shell height (H) and diameter (D).

northeastern New Caledonia. It was found in
areas with rainfall ranging fom 1500 to
3500 mm a year.

Palaina nissidiophila occurs only in the
Belep Islands and along the northwestern
coast of New Caledonia. It attains the smallest
sizes found. It is restricted to areas with low
rainfall (1125 to 1275 mm rain a year). The
species varies enormously in shape.

Palaina perroquini is the largest New Cale-
donian species. It is restricted to the region
south of the great southern mountain mass,
with high rainfall (from 2750 to 3125 mm rain
a year).

Palaina obesa and P. nanodes are both
very small and very stout species showing a
very restricted endemism in regions with high
rainfall, the former in the northeastern moun-

188 TILLIER

size
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20
15
10
5
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tain range and the latter in the southeastern name), and the latter in Mare, Loyalty Islands.

border of the mainland. Palaina sp., seemingly endemic in Adio but
Palaina kuniorum and P. mareana are both known from only two specimens, will be dis-

insular endemics, the former in the Isle of | cussed in the systematic section.

Pines (for which Kunié is the Melanesian Note that species that are most restricted in

NEW CALEDONIAN DIPLOMMATINIDS 189

shape

3.03
2.68
2.33
1.98 |
1.63
"+ .
4 ` ` ©
ея Е
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A € an © O
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FIG. 10. Shape range of New Caledonian species of Palaina.

geographic distribution have a very narrow
rainfall range, which was not immediately
obvious because of the enormous variation of
rainfall over very short distances. Conversely,

Palaina mariei, which is the most widely dis-
tributed species, tolerates the widest rainfall
range. Palaina nissidiophila occupies a rela-
tively wide geographic range although re-

190 TILLIER

rainfall

3500
3000
2000
1000

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DS ° < ~
4 o e <
> o © e
о © о © ©
= г a o
о © “ ©

FIG. 11. Rainfall range of New Caledonian species of Palaina.

stricted to low rainfall, but is found over the
largest homogeneously dry region of New
Caledonia.

Rainfall and shell shape

By tracing on Fig. 8 the scatter of each
population for H versus D, instead of the scat-
ter of each species, it seems that the lower
scatters represent populations collected in
high rainfall areas, and that the upper scatters

represent populations collected in low rainfall
areas. In other words, it seems that stout
shells are found in wetter areas than slender
shells (the diagram is not reproduced here
because it would be unreadable at a size
compatible with printing). To check this, a fac-
tor analysis of the contingency table of the
variables of shape (HS = H/D) and rainfall
(PL) was made using the ANACOR program.
This table was established with the modalities
HS as lines and the modalities PL as col-

NEW CALEDONIAN DIPLOMMATINIDS 191

umns, and by counting the specimens at each
intersection. The class limits corresponding to
each modality are given in Tables 3 and 4.

The result of the analysis is shown in Fig.
12. This projection represents 92% of the
inertia of the scatter, and the other axes do
not change the relative position of the vari-
ables. On this projection the axis 2 quite clear-
ly separates low levels of rainfall and elongat-
ed shells, on the right side, from very high
levels of rainfall and very stout shells well
grouped at the extreme left. The complemen-
tary projection of the individuals does not
show the predominance of any particular spe-
cies on this result, and thus it may be said that
in New Caledonian Palaina, the occurrence of
very stout shells is linked to very high rainfall,
whereas the occurrence of slender shells is
linked to low rainfall. Rainfall probably repre-
sents the degree of moisture of the environ-
ment.

A similar analysis was made for size (HD)
and rainfall. It showed a linkage between very
high rainfall and extreme sizes, but no general
conclusion can be deduced about the selec-
tive action of rainfall on size because very
large and very small species are not scattered

—HS1

and appear weighted as species more than as
individuals.

Clines

If the scatter of each population is traced on
a H versus D diagram, two species exhibit
obvious clines for size. The size of Palaina
nissidiophila increases regularly from the ex-
treme north to the south, between the Belep
Islands (sta. 1) and the Fatenaoue valley
(sta. 14); the shape of the shells is also gradu-
ally transformed. The size of Palaina
montrouzieri also increases from the north-
western Tiébaghi mountain (sta. 4) to the
southeastern Lindéralique (sta. 11) through
stations 9 and 10.

To understand these clines and to try even-
tually to discriminate less obvious ones, a
factor analysis of the species represented by
a large number of specimens over a large
area was done. These species are Palaina
montrouzieri (п = 129 specimens), Р.
nissidiophila (n = 156), P. mariei (n = 282),
P. boucheti (n = 108), and P. opaoana (n =
193). The variables analysed were shell
shape (HS), shell size (HD), and rainfall (PL).

axis2

HS 10

HS9

PL2

HS5

axis 1

HS7 use

PL1
HS8

FIG. 12. Factor analysis of the contingency table of the variables rainfall (PL) and shape (HS). Projection of
the variables. Axis 1: proper value 0.38, inertia 66%; axis 2: proper value 0.15, inertia 26%.

TILLIER

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NEW CALEDONIAN DIPLOMMATINIDS 193

The station numbers (used because they
make an analysis much easier than coordi-
nates) were introduced as supplementary
columns, which means that they do not influ-
ence the analysis but are projected on the
diagrams. The class limits for each modality in
each species are given in Table 5.

The projection of the variables for Palaina
nissidiophila is shown in Fig. 13. The cline for
size from north (sta. 1) to south (sta. 14) is
clearly shown, and appears to be linked to
increase of rainfall. In the northern part of the
range (stas. 1-6) stouter shells are found in
higher rainfall, but in the southern part of the
range (sta. 14) the shells become more
slender whereas rainfall increases. This ap-
parent aberration will be analysed further.

| can analyze the variations of Palaina
montrouzieri only over the northern half of
New Caledonia (it is known from the southern
half only from the type-specimen). The pro-
jection in Fig. 14 shows a correlative variation
of shell size and shell shape from stout small
shells to large slender shells. Along axis 1,
relatively small shells are associated with
lower rainfali whereas the relatively large

shells are associated with relatively high rain-
fall. The very high rainfall PL5 is opposed to
all the lower rainfalls along axis 2. The in-
terpretation, with stations, is a very clear cline
for size and shape from the Tiébaghi to
Lindéralique (stas. 4, 9, 10, 11) related with
the increase of rainfall. Inside this cline sev-
eral clines for shape are induced by very high
rainfall at stations 8, 17 and 20, which are all
on mountains where rainfall is much higher
than in surrounding lowland area. The
Pombei specimens (sta. 13) have a stout
shape linked to high rainfall, but are abnor-
mally large; that is why station 13 is farther left
on the diagram than the other equivalent sta-
tions. A tentative explanation will be given
later.

Palaina mariei is, at first sight, a different
case compared with the two preceding spe-
cies. When examining the scatter of the dif-
ferent populations on a H/D diagram, varia-
tions look geographically random and no
clines are obvious except over a very short
distance, which raises doubt about interpreta-
tion. However, the projection of the variables
on the (1, 2) plane as shown in Fig. 15 is

axis 2

axis!

FIG. 13. Factor analysis of P. nissidiophila for rainfall (PL), size (HD) and shape (HS); projection of the
variables and of the stations. Axes 1 and 2 have respectively 0.88 and 0.57 as proper values and represent

26% and 17% of the variance.

194 TILLIER

axis2

FIG. 14. Factor analysis of P. montrouzieri for rainfall (PL) size (HD) and shape (HS); projection of the

variables and of the stations. The axes 1 and 2 have each 0.72 and 0.53 as proper values and represent 20
and 15% of the variance.

clear. Large and slender shells are associated work, the clines caused by the same mechan-
with very low rainfall, small and stout shells ism as the preceding ones cannot be ob-
with high rainfall and very stout shells with served over a distance exceeding a few
very high rainfall. As the species occupies a tenths of a kilometer and, as a result, geo-
geographic range exhibiting a climatic patch- graphic variations look random.

NEW CALEDONIAN DIPLOMMATINIDS 195

axis!

FIG. 15. Factor analysis of P. mariei for rainfall (PL), size (HD) and shape (HS); projection of the variables.
The axes 1 and 2 have each 0.64 and 0.49 as proper values and represent 16% and 12% of the variance.

Palaina boucheti (Fig. 16) shows the same
trends as P. mariei. A cline of increasing sizes
from high to low rainfall is seen, together with
a cline for shape associating the two stoutest
classes with the two highest rainfalls and the
three most slender classes with the two low-
est rainfalls.

A similar diagram for Palaina opaoana is
impossible to interpret, except for the associa-
tion of large sizes and high rainfall. This may
be due not only to large differences in sample
sizes (50% of the specimens in a single sta-
tion), but also to interaction with Palaina
montrouzieri.

In conclusion it may be said that rainfall
(and thus moisture) influences both size and
shape. Its effect on shape is constant, but size
increases with rainfall in some species and
decreases in some others. Rainfall possibly
does not directly influence shell size. This ac-
tion of rainfall may explain the large clines in
the northern mainland where climatic change
is continuous over large distances, as the ap-
parent random variation which is found further
south and east; the latter being in fact clines

over small distances. However, influence of
rainfall does not explain all the observed
variation. The hypothesis involving species
interaction will now be explored.

Interaction of species and character
displacement

Peake (1973) remarked that sympatric
species of Solomon Islands diplommatinids
do not overlap morphologically. Fig. 8 shows
that, in New Caledonia, there are large zones
of overlap of the morphological scatter of the
species when all populations are considered.
However, there is not one case where there is
morphological overlap where species were
collected together. The data on allopatry and
sympatry are summarized in Table 2. The
species which converge when allopatric and
diverge when sympatric are: 1) Palaina
nissidiophila and P. mariei in station 14; 2) P.
mariei and P. boucheti in stas. 20, 50, 51, 52;
3) P. opaoana and P. mariei in stas. 21, 22,
27, 28; 4) P. montrouzieri and P. opaoana
were found only to be allopatric, but in the

196 TILLIER

FIG. 16. Factor analysis of P. boucheti for rainfall (PL), size (HD) and shape (HS); projection of the variables.
The axes 1 and 2 have respectively 0.62 and 0.45 as proper values and represent 19% and 14% of the

variance.

same geographic range. Palaina obesa and
P. nanodes were found sympatric with only
much larger species.

In most cases it is the size scatter of the
populations which appear reduced to avoid
the overlap. An example is given for Ра/ата
ораоапа and P. mariei in Nindiah (sta. 22) as
illustrated in Fig. 14. The displacement of size
caused by sympatry may also be the origin of
the aberrant position of station 13 (Pombei) in
Fig. 11. In the cline of Palaina montrouzieri,
this station appears to be a good intermediate
between dry and wet stations of the northeast-
ern coast, but shell size is larger than ex-
pected there. This may be related with the fact
that the largest Ра/ата boucheti were found
in this station, fitting in their cline for size and
rainfall.

In only one case do we have evidence for
character displacement in shape. As seen in
Fig. 10, Palaina nissidiophila has a clinal
variation from northern small sizes to south-

ern larger sizes, correlated with a normal vari-
ation of the shell shape in the northern part of
the range which abnormally reverses in the
southern part. Between the region of Koumac
(stas. 5, 6) and the Faténaoué valley (sta. 14),
shells were expected to become stouter as
rainfall increases but become more slender.
In fact, as shown in Fig. 18, the place where
the cline for shape reverses is the northern
limit of the area of Palaina mariei, the scatter
of which on a H/D diagram is the one which
would have been expected for P. nissidiophila
in this region.

Two solutions may be proposed here to ex-
plain these character displacements. If we
admit that competition for food occurs, which
is quite possible as far as all species have the
same radula, differences in shell shape
and/or size could allow sympatric species
to exploit different sizes of interstices in the
same leaf litter; or the presence of several
species in the same leaf litter could cause

NEW CALEDONIAN DIPLOMMATINIDS 197

2.5

0.9 1

Dmm
1.2

FIG. 17. Reduced scatter of H and D in sympatric P. opaoana and P. mariei from Nindiah (sta. 22). Compare

with the scatter of the whole species, Fig. 8.

them to live outside of their optimal range of
moisture, so that different shell shapes or
sizes would be selected. On the other hand,
males have no penis and if individuals do not
recognize each other chemically for mating
(which we do not know), we can postulate that
they recognize each other by shell shape and
size. Thus the animals having the same
shape and size, but belonging to different
species, would be less successful in repro-
duction, often mating with the wrong partners,
and would be eliminated generation after
generation, provoking the morphological di-
vergence of sympatric populations. Of course
the observed character displacements can
also be the result of the combination of factors
proposed here as well as some others that we
do not suspect.

As character displacement seems so com-
mon, the observed clinal variations in New
Caledonian diplommatinids could be the re-

sult of coevolution of species having adjacent
scatters for H and D. The final and purely
theoretical stage of such a coevolution, which
can never be attained because environment
is not constant through time, would be the
establishment of parallel clines of all species
over all of mainland New Caledonia. Severa!
tests have been made to try to demonstrate
the interdependency of the clines of the vari-
ous species, this interdependency being in-
terpretable as the result of such an evolution-
ary process. Unfortunately, and as only factor
analysis could be accepted for methodologi-
cal reasons explained earlier, the results were
not more conclusive than the simple H/D dia-
grams. However two remarks can be made:
First, the clines of Palaina mariei and P.
boucheti, which both occur over nearly all the
mainland, are roughly parallel (Figs. 15, 16),
so that identical shells are found in both spe-
cies, but in different environmental conditions:

198 TILLIER

0.7 0.8 0.9

1 1.1 1.2 D mm

FIG. 18. Character displacement in shell shape of P. nissidiophila.. Clinal scatter from sta. 1 to sta. 14 in full
lines; scatter of P. mariei, sympatric with P. nissidiophila in sta. 14, in dotted line.

that is shown by the shells of the Figures 211
and 24B-24D, but the P. mariei shell comes
from the extreme south whereas the P.
boucheti shells come from the extreme north.
Secondly, Palaina montrouzieri and P.
ораоапа seem to exclude each other over the
entire geographic range of the latter. In cen-
tral western New Caledonia, only Palaina
ораоапа was found at low altitudes and only
P. montrouzieri was found at high altitudes.
Shapes correlated with the rainfall found in
this region are missing in the H/D diagram of
P. montrouzieri (Fig. 8), and we have seen
that no interpretable cline is found in the
known material of P. opaoana. This could
indicate species interaction on a large scale.

Implications for diplommatinine systematics

As the shells vary so enormously, no one
considering only a few samples representa-
tive of the extreme forms would hesitate to
consider them as belonging to different spe-
cies. As nearly all diplommatinine species
have been described from single samples, it
is probable that a large proportion of the spe-
cific names are synonyms.

It has already been demonstrated that four
states are found in female genital apparatus.
These four states probably represent four
steps of the same evolutionary process but,
although | believe that this process is the loss
of the seminal receptacle, | have no argument

NEW CALEDONIAN DIPLOMMATINIDS 199

which proves that it is not the acquisition of
the receptacle. The steps of this process are
found in all parts of Melanesia, and probably
over the entire range of the Diplommatinidae.
On the other hand, the species found in one
region look more similar to each other than to
the species found elsewhere. For example,
nine Solomon Islands species have a mean
H/D ratio of about 1.94, whereas New Cale-
donian species have a mean H/D ratio of
about 2.16. Because we know that this ratio
depends on rainfall in New Caledonia and be-
cause the Solomon Islands are wetter than
New Caledonia, it is not possible to use this
apparent general dissimilarity as a supraspe-
cific character. Thus, in the Diplommatina-
Palaina group, we have no argument, either
anatomical or conchological, to determine
what is convergence and what is monophy-
letism and as a result cannot at the moment
discriminate any supraspecific group.

DESCRIPTION OF SPECIES

In the lists of materials, each sample is de-
fined by the number of the station (locality
indicated in Table 1 and Fig. 7) and the num-
ber of specimens in brackets. The abbrevia-
tions used are: AMS, Australian Museum,
Sydney; MNHN, Museum national d'Histoire
naturelle, Paris; NMNZ, National Museum of
New Zealand, Wellington.

Palaina montrouzieri (Crosse, 1874)
Figs. 19, 20

Diplommatina montrouzieri Crosse, 1874a:
110; Crosse, 1874b: 394, pl. 12, fig. 8 (Baie
du Sud).

Palaina montrouzieri (Crosse), Franc, 1957:
41, pl. 4, fig. 48; Solem, 1961: 427; Kobelt,
1902: 401.

Diplommatina sp., Hedley, 1898: 103, fig. 11
(Oubatche).

Holotype: Baie du Sud, MNHN; Fig. 19B.

Other material: sta. 4 (12), sta. 8 (1), sta. 9
(> 50), sta. 10 (27), sta. 11 (> 50), sta. 13 (4),
sta. 20 (4), sta. 17 (2).

Preserved material: sta. 4, sta. 10, sta. 11,
sta. 13, sta. 20.

Geographic range: probably nearly all of
New Caledonia, except the northern point and
the western coastal border; possibly absent
from the Mt. Guemba southeastern coastal

FIG. 19. Shells of Palaina montrouzieri. Scale line
1 тт. A, Aoupinié (sta. 17); В, holotype, Baie de
Prony (sta. 51); C, Paéoua (sta. 20); D and E,
Tiebaghi (sta. 4); F, Kaala (sta. 9); G and H,
Lindéralique (sta. 11); |, Kavatche (sta. 10).

FIG. 20. Female genital anatomy of P. montrou-
zieri. Scale line 0.5 mm. A, Pombei (sta. 13); B,
Lindéralique (sta. 11); С, Tiébaghi (sta. 4). BC,
bursa copulatrix; O, oviduct; R, rectum; SR, semi-
nal receptacle; U, uterus.

200 TILLIER

range. Although we did not collect it farther
south than the Aoupinie (sta. 17), we have no
reason to doubt the accuracy of the type local-
ity.
Shell (Fig. 19): from 1.45 x 3.3 mm in
Linderalique (sta. 11) to 1.05 x 2.1 mm in the
Tiebaghi (sta. 5) through a geographic cline.
Stouter in the central range (Aoupinie), at
high altitude in the western mountain masses
(Paeoua) and in the southernmost region
(Baie de Prony): from 1.4 x 2.4 mm to 1.24 x
2 mm. A small columellar tooth present in the
northeastern: coast samples, absent else-
where. Radial ribs always slightly oblique,
crowded at the middle, only slightly more
crowded in the body whorl; more spaced in
Lindéralique (sta. 11), closer when going far-
ther from this locality in any direction.

Female genitalia (Fig. 20): bursa copulatrix
rising upwards from the oviduct, with a nearly
spherical head. Seminal receptacle a small
elongated pouch, appressed along the bursa
stalk but opening independently into the ovi-
duct.

m
Y)

FIG. 21. Shells of Palaina mariei. Scale line 1 mm.
A, Kaala (sta. 9); В, Nekliai (sta. 21); С, Poindimie
(sta. 15); D, Plaine aux Gaiacs (sta. 23); E, Goipin
(sta. 18); Е, Мате (sta. 44); G, lectotype, Nouméa
(sta. 41); H, Baie de Prony (sta. 51); I, Mt. Oungoné
(sta. 52).

Recognition: the only New Caledonian
species with the seminal receptacle opening
into the oviduct. Shell dimensions overlapping
with those of Ра/ата mareana, P. kuniorum,
Р. opaoana and probably P. mariei. The latter
is only smaller, and without anatomical data
the distinction between the largest P. mariei
and the smallest P. montrouzieri is delicate in
the regions where they are potentially sym-
patric (see the case of the Nindiah population
here attributed to P. mariei). P. mareana and
P. kuniorum are always allopatric with P.
montrouzieri; the former is more regularly
conical, with more impressed sutures, more
convex whorls and radial ribs much more
spaced. P. kuniorum has the body whorl more
constricted and has also radial ribs more
spaced, particularly on the upper whorls, al-
though less than in P. mareana. P. opaoana
is potentially. sympatric with P. montrouzieri
and have about the same size. Apart from the
anatomical differences, it is in most cases
easily recognized by its radial ribs largely
spaced on the first whorls and crowded on the
last ones.

Remark: Franc’s (1957) drawing of the
holotype, “voluntarily” (sic) drawn without a
camera lucida, is very different from the speci-
men, here depicted in Fig. 19B.

Palaina mariei (Crosse, 1867)
Figs. 21, 22

Diplommatina mariei Crosse, 1867: 179, pl. 7,
fig. 6 (Nouméa).

Palaina (Cylindropalaina) mariei (Crosse),
Kobelt, 1902: 408; Franc, 1957: 41, pl. 4,
fig. 49; Solem, 1961: 428.

Palaina montrouzieri маг. humilior Cockerell,
1930: 20, fig. 2; Solem, 1960a: 5; Solem,
1961: 428 (near Bourail).

Lectotype (here designated): Nouméa (sta.
41), ММНМ; fig. 21G.

Paralectotypes: 2 specimens labelled “var.
type” by Crosse + 1 shell from H. Fischer ex
Crosse ex Marie, 1966—all in MNHN.

Other material: sta. 9 (50), sta. 10 (12), sta.
14 (5), sta. 15 (3), sta. 18 (2), sta. 19 (2), sta.
20 (2), sta. 21 (36), sta. 22 (39), sta. 23
(>50), sta. 24 (3), sta. 28 (40), sta. 26 (1),
Sta. 27 (2), sta. 31 (6), sta. 32 (1), sta. 33 (6),
sta. 38 (1), sta. 39 (numerous juv.), sta. 40
(2), sta. 42 (2), sta. 44 (2), sta. 49 (3), sta. 50
(1), sta. 51 (13).

Preserved material: sta. 9, sta. 15, sta. 18,
sta. 19, sta. 21, sta. 24, sta. 27, sta. 28, sta.
31, sta. 39, sta. 42, sta. 44, sta. 49.

NEW CALEDONIAN DIPLOMMATINIDS 201

FIG. 22. Female genital anatomy of P. mariei. Scale
line 0.5 тт. А and В, Ме Maoya (sta. 28); С, Baie
Tina (sta. 42); D, Col des Roussettes (sta. 26). BC,
bursa copulatrix; О, oviduct; В, rectum; SR, semi-
nal receptacle; U, uterus.

Geographic range: nearly all the mainland,
except possibly the northern point and the
northeastern mountain range. Frequent along
the coastlines, rather uncommon in the cen-
tral and southern ranges.

Shell (Fig. 21): dimensions varying from 1.1
x 2.4 mm to 0.8 x 1.6 mm probably through
numerous Clines. Stouter in the southernmost
mainland, with dimensions reaching 1 x
1.8 mm to 0.86 x 1.7 mmon the Mt. Oungone
(sta. 52). А columellar tooth generally present
farther north than Bourail, absent farther
south. Radial ribs as in P. montrouzieri; more
spaced along the western coast, closer when
going eastwards, or southwards’ from
Nouméa.

Female genitalia (Fig. 22): the basal part of
the stalk of the bursa copulatrix prolongs the
distal oviduct from which the proximal oviduct
diverges inwards and upwards. The upper
part of the stalk, which is longer than the basal
one, bends back along the distal oviduct in
such a way as the more or less inflated bursa
head is appressed against the proximal end of
the uterus. The seminal receptacle is a swell-
ing which prolongs the basal part of the bursa
stalk outside of the bend of the latter. Two
dispositions are found: farther north than the
Col des Roussettes (sta. 27), the basal part of
the bursa stalk is parallel to the spire; farther
south, it is bent downwards.

Recognition: only Palaina obesa has a sim-
ilar female genital anatomy in New Caledonia.
It is found only in the northeastern range, is
smaller and has more spaced radial ribs on
the upper whorls. The dimensions of the
shells of P. mariei overlap with those ob-

served in P. opaoana, P. boucheti and P.
nissidiophila, but it was found sympatric with
all three. The former is generally larger, never
has a columellar tooth, and has more widely
spaced ribs on the upper whorls. P. boucheti
is generally smaller, more cylindric and has
closer radial ribs on the upper whorls. P.
nissidiophila has a shape varying from
cylindrical to conical, but its sutures are less
impressed and its whorls less convex than
those of P. mariei; it also has much closer
radial ribs, and a more oblique aperture.

Remarks: the specimen labelled by Crosse
“var. В” is here selected as the lectotype be-
cause the two shells labelled “уаг. type” are
very badly preserved.

No preserved specimen was obtained from
Nindiah (sta. 22), and this sample could have
been attributed to P. montrouzieri. lt is here
identified as P. mariei because shell dimen-
sions are closer to those of the P. mariei
found in the same region. If it proves to belong
to P. montrouzieri, the character displace-
ment shown in Fig. 14 would be much greater
than proposed here.

Palaina obesa (Hedley, 1898)
Fig. 23

Diplommatina obesa Hedley, 1898: 102, fig.
10 (Oubatche).

Palaina (Macropalaina) obesa (Hedley),
Kobelt, 1902: 410; Franc, 1957: 41-42, pl.
4, fig. 50.

Palaina obesa (Hedley), Solem, 1961: 428.

Type material (not seen): Oubatche, AMS
(sta. 8).

Other material (preserved): sta. 7 (3).

Geographic range: northeastern range (=
Chaine du Panié).

Shell (Fig. 23A, C): from 1.4 x 0.75 mm to
1.6 x 0.8mm, very stout. Columellar tooth
present or absent. Radial ribs distinctly more
widely spaced on the upper whorls than on
the following ones.

Female genitalia (Fig. 23B): bursa stalk
straight and rather short, perpendicular from
the oviduct upwards. The seminal receptacle
is a very short pouch, prolonging the distal
oviduct through the basis of the bursa copula-
trix. It opens into the stalk, and not directly into
the oviduct.

Recognition: Palaina obesa is distinct from
both P. mariei and P. boucheti by its female
genital anatomy. A similar disposition is found
in P. mariei but the portion of the bursa stalk
between the oviduct and the seminal recepta-

202 TILLIER

FIG. 23. Palaina obesa, Mandjelia, sta. 7. Scale
line 1 mm. A and С, shells; В, female genital anat-
omy. BC, bursa copulatrix; G, gonad; O, oviduct; R,
rectum; SR, seminal receptacle; U, uterus.

cle is much shorter in P. obesa. The shell
differs from the shell of P. mariei by its smaller
size and by the more widely spaced radial ribs
of the upper whorls. P. obesa is convergent
with the smallest P. boucheti, except for the
anatomy and the spacing of the ribs; but the
latter reaches its maximum size in the north-
eastern region where it is potentially sympat-
ric with the much smaller P. obesa.

Palaina boucheti Tillier, n.sp.
Figs. 24, 25

Holotype: Me Ori, 530 m, P. Bouchet coll.
30.4.1979 (sta. 29), MNHN.

Paratypes: 11, same locality.

Other material: sta. 12 (14), sta. 13 (10),
sta. 16 (1), sta. 20 (4), sta. 36 (1), sta. 45 (1),
sta. 46 (3), sta. 47 (8), sta. 48 (12), sta. 50
(34), sta. 52 (4), sta. 51 (4).

Preserved material: type locality, sta. 12,
sta. 13, sta. 20, sta. 46, sta. 47, sta. 48.

Geographic range: central New Caledonia
farther south than Kaala-Gomen; absent from
the western coastal plains and probably from
the eastern coastline; probably replaced by
P.obesa to the northeast of its range. Littoral
only around the southernmost range, from the
Ouinné river to the Baie de Prony.

Shell (Fig. 24): from 0.86 x 1.7 mm to 0.75
x 1.4 mm in the type series, reaching 1 x
1.7 mm to 0.86 x 1.8 mm elsewhere. Gener-
ally smaller and more cylindric than P. mariei.
A columellar tooth present or absent in north-
ern New Caledonia (Taom sta. 12, Pombei
sta. 13, Paéoua sta. 20), always absent far-
ther south.

Female genitalia (Fig. 25): no seminal re-
ceptacle. The bursa stalk goes downwards
from the oviduct. Two dispositions are found:
in western samples (sta. 20, sta. 12, sta. 29),

Ch)

OP Я
=

FIG. 24. Shells of Palaina boucheti. Scale line
1mm. A, Taom (sta. 12); В and С, Paéoua (sta.
20); D, Pombei (sta. 13); E, Mt. Guemba (sta. 47);
F, Touaourou (sta. 48); С and H, Ме Ori (sta. 29,
paratypes).

FIG. 25. Female genital anatomy of P. boucheti.
Scale line 0.5mm. A, Paéoua (sta. 20); B,
Touaourou (sta. 48); С, Taom (sta. 12); D, Pombei
(sta. 13). BC, bursa copulatrix; O, oviduct; R,
rectum; U, uterus.

the basal part of the stalk runs parallel to the
spire before bending upwards back to the
proximal uterus, whereas in the eastern sam-
ples (sta. 13 to Touaourou sta. 48), the basal
part of the stalk goes downwards parallel to
the shell axis before bending back.
Discussion: the largest Palaina boucheti
have shells completely convergent with the
smallest P. mariei (Figs. 211, 24D) but in dif-
ferent environmental conditions and in differ-
ent parts of the common range of the two spe-
cies. In such cases, dissection is necessary to
check the presence or absence of a seminal
receptacle. The dimensions of P. boucheti
also overlap with those of P. nissidiophila
which was never found sympatric with it, be-

NEW CALEDONIAN DIPLOMMATINIDS 203

ing a species found in dry environments in
northwestern New Caledonia. P. boucheti
has much more impressed sutures and
rounded whorls, and much less crowded ra-
dial ribs.

Palaina nissidiophila Tillier, n.sp.
Fig. 26

Holotype: Nienane (Iles Daos du Nord),
Bouchet and Chérel coll., 23.8.78 (sta. 3),
MNHN; Fig. 26B.

Paratypes (all dry): 9, same locality.

Other material (all dry): sta. 1 (50), sta. 2
(1), sta. 5 (21), sta. 6 (25), sta. 14 (50).

Geographic range: from Pott (Belep
Islands) to the Koniambo mountain through
Art, the Daos du Nord Islands, the northern
point (probably) and the northwestern coastal
plains.

Shell (Fig. 26): from 0.65 x 1.4 mm in Pott
(sta. 1) to 0.85 x 1.8mm in Koum (sta. 6)
through a geographic cline, reaching 0.9 x
2.2 mm farther south. Suture not impressed
and whorls generally only slightly convex;
shape nearly cylindrical from Pott to Koum,
becoming an elongated cone farther south. A
small columellar tooth present in Le Cresson
(sta. 5), present or absent in Koum (sta. 6),
absent elsewhere. Peristome thicker than in
other New Caledonian species, always
oblique. Radial ribs always very crowded.

Discussion: the non-impressed sutures and
the crowded ribs make P. nissidiophila easy
to recognize. It is sympatric with P. mariei
south of Koum (sta. 6) to the Koniambo (sta.
14) and thus there is no doubt about their
specific distinction. Without anatomical data,
there are less arguments for considering it as
specifically distinct from P. boucheti which is
always allopatric with it. The reason which
makes me consider P. nissidiophila a distinct
species is the large gap between it and P.
boucheti in ornamentation and whorl contour.
Geographically, they are found near one
another.

Palaina nanodes Tillier, n.sp.
Fig. 27

Holotype: Touaourou, 10 т, Bouchet coll.
8.12.1978 (sta. 48), MNHN.

Paratypes (8 preserved): 17 specimens,
same sample.

Geographic range: P. nanodes was found
only in Touaourou, but probably occurs along

FIG. 26. Shells of Ра/ата nissidiophila. Scale line
1 mm. A, Pott (sta. 1); В, Holotype, Nienane (sta.
3); C, Le Cresson (sta. 5); D and E, Koum (sta. 6);
F, Faténaoué (sta. 14).

Am)
Cy
A B

Fig. 27. Palaina nanodes Tillier, n. sp. Scale line A,
1 тт; В, 0.5 mm. A, shell; В, Female genital anat-
omy; both paratypes from Touaourou (sta. 48).

the coast, on the upraised reef between Yate
and Goro. At least one much bigger Para-
rhytida has the same odd range.

Shell (Fig. 27A): probably the smallest of all
described Palaina-Diplommatina species,
from 0.6 x 1.05mm to 0.7 x 1.38 mm.
Otherwise looks like a very small P. boucheti,
but has closer radial ribs. Columellar tooth
present or absent.

Female genitalia (Fig. 27B): no seminal
receptacle. A very short portion of the bursa
copulatrix stalk prolonging the distal oviduct,
a much longer portion bent back upward to
the proximal end of the uterus. A small round-
ed bursa head.

Discussion: there is no overlap for dimen-
sions with any other New Caledonian species.
The smallest P. nissidiophila are more slen-
der (but found in drier conditions), with less
impressed sutures, and P. nanodes was
found sympatric with P. boucheti.

204 TILLIER

Palaina kuniorum Tillier, n.sp.
Fig. 28

Holotype: Ouro, lle des Pins, Bouchet coll.
21.10.1978. (sta. 53), MNHN; Fig. 28B.

Paratypes (all dry): 13, same sample.

Geographic range: lle des Pins (called
Kunié by Melanesians).

Shell (Fig. 28): in the only population col-
lected, dimensions from 3.5 x 1.45 тт to 3
х 1.3 тт. Holotype 3.35 x 1.4 тт. No col-
umellar tooth. Radial ribs rather widely
spaced, closer on the body whorl. Body whorl
distinctly constricted.

Discussion: the dimensions of P. kuniorum
overlap those of P. mareana, which is easy to
recognize by its more convex whorls and
regularly conical shape. It seems closer to P.
montrouzieri, from which it differs only by its
more widely spaced radial ribs and more dis-
tinctly constricted body whorl. On the other
hand the constriction of the body whorl is a
variable character, but the form of P.
montrouzieri from Linderalique (sta. 11; Fig.
19G, H), which is the closest to P. kuniorum
by its loose radial ribbing, has a more regu-
larly conical shape (both are found on cal-
careous soils: does this allow а faster
growth?). All the specimens of P. montrouzieri
approaching P. kuniorum by their shell char-
acters come from northern New Caledonia,
but we know only the holotype as coming from
the southern regions and may suspect that it
is not very representative of the southern
populations of P. montrouzieri. Lastly, there is
a low probability for P. montrouzieri to occur
along the coast of the mainland between Yate
and the Baie de Prony, that is the closest to
the lle des Pins and where P. Bouchet already
collected four species. All these arguments

FIG. 28. Palaina kuniorum п. sp. Scale line 1 mm.
Ouro, Isle of Pines (sta. 53). A, paratype; B, Holo-
type.

are contradictory, and the status of P. kuni-
orum, species or subspecies, will remain
dubious as long as its female genital anatomy
is not known. | have considered it a species
because it could as well be related to P.
ораоапа, P. mareana, Palaina sp. or even to
P. perroquini as conchological characters
prove to be so variable.

Palaina perroquini (Crosse, 1871)
Fig. 29

Diplommatina perroquini Crosse, 1871: 204;
1873: 44, pl. 12, fig. 8 (New Caledonia).
Palaina (Macropalaina) perroquini (Crosse),
Kobelt, 1902: 410; Franc, 1957: 42, pl. 4,
fig. (51%

Palaina perroquini (Crosse), Solem, 1961:
428.

Type material: the specimen depicted by
Franc as the holotype, here redrawn in Fig.
29A, is probably not even type material: judg-
ing from the label it was given by Marie to
Crosse in 1873, and we do not know whether

FIG. 29. Palaina perroquini. Scale line 1 mm. A and
B, Baie de Prony (sta. 51) (A = specimen depicted
as the holotype by Franc); C, Mt. Guemba (sta. 47).

NEW CALEDONIAN DIPLOMMATINIDS 205

Crosse had seen it previous to his first de-
scription in 1871. Two other samples, contain-
ing fifteen shells, are housed in the MNHN as
acquired by Crosse from Petit in 1874. They
are possibly syntypes, collected by Perroquin
and given to Petit before 1871, and then
acquired by Crosse, but we have no evidence
to confirm that Crosse had seen them before
his first description of the species. If neces-
sary, Franc’s “holotype” should be selected
as a neotype, but P. perroquini is so easy to
recognize that a neotype is not needed.

Other material: sta. 43 (1 + juv.), sta. 47 (4
+ juv.), sta. 48 (3 + juv.), sta. 51 (14), plus
about ten shells without accurate locality.

Preserved material: sta. 43, sta. 47, sta. 48.

Geographic range: southeasternmost part
of the mainland, from the Yate river to the Baie
de Prony through the Plaine des Lacs, and
further east to the coastline.

Shell (Fig. 29): from 1.5 x 3mm to 1.85 x
4 mm. Regularly conical when tall, with penul-
timate whorl slightly inflated when short. Body
whorl slightly constricted. No columellar tooth.
Radial ribs sigmoid on the upper whorls,
forming wing-like expansions in juveniles but
more or less eroded in adults; more crowded
on the last and often on the penultimate whorl.

Female genitalia: full adult not seen. In sub-
adult females, the developing bursa copulatrix
seems to be similar to the bursa found in P.
mareana (Fig. 32), but | cannot be sure that
there is no seminal receptacle at all outside of
the bend of the bursa stalk, as is found in
some Solomon Islands species and in the
Australian Palaina strangei (Tillier, unpub-
lished).

Recognition: the size, shape and sigmoid
radial ribs of P. perroquini are not found in
any other New Caledonian diplommatinid.

Palaina opaoana Tillier, n.sp.
Figs. 30, 31,.32

Holotype: junction of the rivers running
down the Ме Maoya and the Pic Poya, alt.
50 m, Tillier and Bouchet coll. 15.6.1979 (sta.
28), MNHN.

Paratypes (preserved): 10, same sample.

Other material: sta. 21 (2), sta. 22 (39), sta.
27 (4), sta. 30 (5), sta. 34 (>200), sta. 35 (5),
sta. 37 (3).

Preserved material: sta. 21, sta. 27, sta. 28
(type locality), sta. 30, sta. 35, sta. 37.

Geographic range: central western New
Caledonia between the latitude of Houailou
and the Dzumac range (the latter is the last

mountain before the southern lowland). Prob-
ably never littoral.

Shell (Figs. 30, 31): from 1.3 x 2.9mm to
1.1 x 2mm; may be stouter, reaching 1.25 x
2 тт on the Dzumac (alt. 1000 т; sta. 37), or
much more slender, reaching 1.1 x 2.6 mm in
the dry Col des Arabes (Figs. 31D, E; sta. 34).
Close to P. montrouzieri by its size and
shape, but the upper whorls more convex.
Radial ribs widely spaced and parallel to the
shell axis on the upper whorls (closer and
oblique in P. montrouzieri), close and slightly
oblique on the following ones.

Female genitalia (Fig. 32): no seminal re-
ceptacle. Bursa stalk going outwards and
downwards from the oviduct before bending
back parallel to the oviduct in the western-
most samples (sta. 37, sta. 28, sta. 21). In
central and eastern samples, the bursa stalk
goes downwards almost perpendicular from
the oviduct and bursa head is in the centre of
the intestinal loop instead of being appressed
against the proximal end of the uterus. The
intermediate position is found in the Col des
Roussettes (sta. 27).

Recognition: differs from P. montrouzieri
and from the largest P. mariei, which may

FIG. 30. Shells of Palaina opaoana Tillier, n. sp.
Scale line 1 mm. A and B, Mt. Dzumac (sta. 37); C,
Col des Roussettes (sta. 27); D and Е, Ме Maoya
(sta. 28); D, paratype; E, Holotype.

206 TILLIER

FIG. 31. P. opaoana. Scale line 1mm. A and B,
Dothio (sta. 30); C, Nassirah (sta. 35); D and E, Col
des Arabes (sta. 34).

converge with it by their dimensions, by the
female genitalia and by the radial ribs of the
upper whorls. By shell size and genital anato-
my, two geographic sets of population can be
distinguished: one western, with larger shells
(Fig. 30), and with the disposition of the bursa
copulatrix shown in Fig. 32A, C; the second
eastern, with smaller shells (Fig. 31) and the
genital disposition shown in Fig. 32B; the
transition is probably found nearby (inter-
mediate found in the Col des Roussettes, sta.
27).

Palaina opaoana resembles the four (?)
New Hebridean species, which have the
same type of shell shape and sculpture, but
whose anatomy is unknown.

Palaina mareana Tillier, n.sp.
Figs. 33, 34

Holotype: Enéné, Mare Island, Bouchet
coll. 7.4.1979 (sta. 54), MNHN.

Paratypes (preserved): 6, same sample.

Other material: sta. 55 (1), sta. 56 (5).

Preserved material: sta. 54 (type locality),
sta. 56.

Geographic range: Mare Island, Loyalty
Islands.

Shell (Fig. 33): from 1.4 x 3.7 mm to 1.2 x
2.8 mm, the largest shells being more regu-

FIG. 32. Female genital anatomy of P. opaoana.
Scale line 0.5 тт. A, Mé Maoya (sta. 21); В,
Nassirah (sta. 35); C, Mt. Dzumac (sta. 37); BC,
bursa copulatrix; G, Gonad; О, oviduct; В, rectum;
U, uterus.

FIG. 33. Palaina mareana Tillier, n. sp. Scale line
1 тт. A and В, Месе (sta. 56); С, Епепе (sta. 54),
paratype.

NEW CALEDONIAN DIPLOMMATINIDS 207

A 2 B

FIG. 34. Female genital anatomy of P. mareana.
Scale line 0.5 mm. Paratypes, Enene (sta. 54); BC,
bursa copulatrix; О, oviduct; R, rectum; U, uterus.

FIG. 35. Shells of Ра/ата sp., Adio (sta. 25). Scale
line 1mm.

larly conical than the smallest ones. Sutures
impressed, whorls convex. Radial ribs always
lamellar, widely spaced, often becoming
slightly more crowded on the body whorl.

Female genitalia (Fig. 34): no seminal re-
ceptacle. Bursa copulatrix long and slender.
Bursa stalk first running parallel to and under
the oviduct and then bent back forwards to the
proximal end of the uterus.

Discussion: distinct from any other New
Caledonian species, the smaller Ра/ата sp.
excepted, by its conical elongated shape,
convex whorls and loose radial sculpture.
Close to the Australian P. strangei in its shell
characters, but the latter has a stouter shell
and a seminal receptacle outside of the bend
of the bursa stalk (Tillier, unpublished).

Palaina sp.
Fig. 35

Material (dry): three shells, the best pre-
served broken, sta. 25.

Geographic range: seems restricted to the
calcareous outcrop of Adio (sta. 25).

Shell (Fig. 35): similar to P. mareana but
smaller, the two preserved shells measuring
2.6 x 1.2 mm and 2.9 x 1.1 mm.

Discussion: although | do not believe it,
these shells could be elongated Palaina
mariei with a loose radial sculpture possibly
due to the occurrence of calcareous rocks;
but P. mariei is found unmodified on such
rocks in Nindiah (sta. 22) and on the south-
eastern upraised coral reef (sta. 45, sta. 49). |
prefer to consider it a species which spread
when calcareous rocks were not eroded and
which is now restricted to the outcrop in Adio.
If the elongated conical shape, convex whorls
and loose sculpture are not correlated with
calcareous rocks, Palaina sp. could be related
with the Australian P. strangei and with P.
mareana.

ACKNOWLEDGEMENTS

| am most grateful to Frédérique Vallee and
Hughes Demongeot, who worked out the sta-
tistical treatment of the data in the Laboratoire
de Statistiques, Universite Pierre et Marie
Curie, Paris. | am also indebted to Professor
A. J. Cain for criticism and advice and to Dr.
G. M. Davis, who reviewed the manuscript.
For the loan of specimens | thank Drs. F.
Climo of the National Museum of New Zea-
land, Wellington, P. Mordan and J. Peake of
the British Museum (Natural History), and W.
Ponder of the Australian Museum, Sydney.

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SOLEM, A., 1960b, Non-marine Mollusca from
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MALACOLOGIA, 1981, 21(1-2): 209-262

DIFFERENT MODES OF EVOLUTION AND ADAPTIVE RADIATION
IN THE POMATIOPSIDAE (PROSOBRANCHIA: MESOGASTROPODA)

George M. Davis!

Academy of Natural Sciences, Nineteenth and the Parkway, Philadelphia, PA 19103, U.S.A.

ABSTRACT

Two subfamilies of the Pomatiopsidae are shown to have different tempos and modes of
evolution. Data for the Triculinae are not new but represent a synthesis of several data sets
(Davis, 1979, 1980; Davis & Greer, 1980). Data for the Pomatiopsinae with emphasis on the
Tomichia radiation of South Africa are new. The distribution of modern pomatiopsid taxa is
vicariant, a relict distribution with a secondary elaboration in Southeast Asia and the Far East
extending to North America. There are eight pomatiopsine genera, one each in South Africa,
South America, and Australia; one genus is found in an arc from western China to the Philippines
and Sulawesi with taxa reaching Japan; two are endemic in Japan; one is found in Manchuria,
Japan, and western U.S.A.; one is endemic in the U.S.A. There are 16 triculine genera, all but
one of which are located entirely in Southeast Asia or western China. Tricula extends in an arc
from India through China to the Philippines and in an arc through Burma to Malaysia.

The Triculinae have undergone an extraordinary endemic radiation in the Mekong River,
yielding three tribes, 11 genera and over 90 species in a period of about 12 million years. This
burst of cladogenesis was apparently driven by extrinsic processes correlated with the massive
tectonics caused by the Himalayan orogeny that led to the formation of the major river systems
of Southeast Asia, and western China. The morphological changes in the entirely aquatic group
of snails that marked the entrance into various new adaptive zones involved a series of innova-
tions in the female reproductive system, the male reproductive system posterior to the penis, and
the central tooth of the radula. Bursts of speciation following each morphological innovation or
series of correlated innovations yielded clusters of species that are considered discrete genera.
The genera are separated by distinct gaps defined by morphological distances that are meas-
ures of morphological changes indicative of entrances into new adaptive zones.

Pomatiopsine taxa are aquatic, amphibious, or terrestrial. Modes of evolution in the
Pomatiopsinae of the southern continents are in marked contrast to those in the Triculinae. In
South Africa there are, at most, eight species of Tomichia with an evolutionary history of at least
80 million years. In Australia there are, at most, nine species of Coxiella. Tomichia and Coxiella
are very similar anatomically. No burst of cladogenesis or considerable speciation is seen.
Species of Tomichia do not differ very much in anatomy. The apparent low rate of speciation and
lack of cladogenesis correlate with the lack of tectonic upheaval and gradual climatic changes
since proto-Tomichia and proto-Coxiella were separated by the breakup of Gondwanaland. The
limited Tomichia radiation is apparently in response to increasing aridity spreading from west to
east in South Africa since the breakup of Gondwanaland. Speciation has not involved morpho-
logical modification but rather, adaptation to different ecological settings: freshwater streams,
freshwater lakes, amphibious ecotones, temporary brackish water pools. Preadapted morpho-
logical features for an amphibious existence were probably the large, powerful foot and the
elongate spermathecal duct.

The tempo of the Mekong River triculine evolution is rapid (R = about 0.40 contrasted with a
slower rate (R = about 0.139) for the Tomichia radiation. The mode of triculine evolution is
rapid, episodic speciation involving considerable morphological innovation and cladogenesis, all
associated with extreme tectonism. The mode of Tomichia evolution involves a physiological
radiation with low morphological diversity associated with gradual climatic change and general
absence of tectonism.

INTRODUCTION In considering tempos | am concerned with

rates of cladogenesis, the number and extent

Modes and tempos of evolution above the of adaptive radiations in phyletically allied
species level are highly relevant topics for clades (per unit time), and the rate of extinc-
contemporary students of biological evolution. tion of species and lineages. By extent of

1Supported by U.S. National Institutes of Health grant №. A1-11373.
(209)

210 DAVIS

adaptive radiation, | mean the number of spe-
cies of a single radiation and the different
niche dimensions these species occupy.

In considering modes of evolution, | am
concerned with how organisms respond to the
selective pressures of different types of
changing environments, and with how organ-
isms respond to different rates of environ-
mental change. The presumption is made that
speciation and evolution above the species
level will not occur in environmental stasis.

The purpose of this paper is to demonstrate
two vastly different modes and tempos of evo-
lution in the rissoacean family Pomatiopsidae.
One mode involves a radiation of consider-
able morphological uniformity but physiologi-
cal divergence in a setting of gradual environ-
mental change. The other mode involves a
radiation exhibiting numerous morphological
innovations associated with rapid tectonic
environmental changes. The most important
comparisons made here involve the extraor-
dinary triculine radiation in the Mekong River
and the more modest Tomichia radiation in
South Africa. Data pertinent for discussing the
triculine radiation have been published
(Davis, 1979, 1980; Davis & Greer, 1980).
Data for the Tomichia radiation are new. Two
different clades are involved, because the
Mekong River radiation belongs to the
Triculinae and Tomichia is a member of the
Pomatiopsinae. Together these two subfami-
lies comprise the Pomatiopsidae as recently
defined (Davis, 1979).

The family Pomatiopsidae

The origin and evolution of the family have
been discussed with emphasis on the adap-
tive radiation of the Triculinae in the Mekong
River (Davis, 1979). The evolutionary topol-
ogy of the family is shown in Fig. 1 based on
the hypothesis that the Pomatiopsidae
evolved and diverged into two Gondawanian
subfamilies prior to the breakup of Pangaea.

Published zoogeographical, morphological,
and paleontological data (Davis, 1979) are
consistent with the following concepts: 1) the
distribution of modern pomatiopsid taxa is
vicariant. There is a relictual distribution in the
southern continents with a secondary elabo-
ration in the Far East extending to North
America (Table 1). 2) Triculinae and
Pomatiopsinae were introduced into the Asian
mainland via the Indian Plate. 3) The patterns

of distribution of Pomatiopsidae throughout
Asia and North America and the direction of
evolution of derived morphological character
states indicate a direction of evolution from
Gondawanaland to Asia (Davis, 1979).

The subfamily Triculinae

The subtending of the Asian continent by
India initiated the Himalayan orogeny begin-
ning in the Oligocene some 38 million years
ago (Molnar & Tapponier, 1975). The orogeny
began at the western end of the mountain
chain and spread eastward as the Indian
Plate rotated, bringing the northeast corner
into contact with the Asian mainland in the
Miocene. As the Tibetan region was lifted
from the sea, drainage patterns were initiated
that became the major rivers of Southeast
Asia and much of China. These are the
Irrawaddy, Salween, Mekong, and Yangtze
rivers. Estuarine and finally fluviatile deposits
were laid down in northern Burma at the end
of the Miocene; in the Pliocene the sediments
of the Irrawaddy River became entirely fresh-
water (Pascoe, 1950).

It is apparent that proto-Triculinae were in-
troduced from the Indian Plate into the newly
forming drainages of the Asian mainland
(Davis, 1979, 1980; Davis & Greer, 1980). All
Triculinae thus far studied are entirely fresh-
water in streams, lakes, and rivers. They ex-
tend in three arcs. One arc extends from north-
western India through China to the Philippines.
The second arc extends from India through
northern Burma and western Yunnan, China
and throughout the Mekong River drainage but
ending in northern Cambodia. The third arc
extends through northern Burma, northwest-
ern Thailand into Malaysia.

Tricula, the genus with the most general-
ized morphology and least derived character
states (Davis & Greer, 1980) is found along
each of these arcs. Taxa with the most de-
rived character states are found endemic in
the Mekong and Yangtze River drainages and
in lakes in Yunnan, China between the rivers
(Davis, 1980; Davis & Greer, 1980). These
derived taxa are Halewisia and Pachydrobia
of the Triculini and all members of the
Lacunopsini and Jullieniini. As shown in Table :
1, of 16 genera and 120 species of Triculinae,
10 genera and 92 species (76.7%) are en-
demic to the Mekong River drainage.

POMATIOPSID EVOLUTION 211

PRESENT

MIOCENE

TRICULINAE

100

120
CRETACEOUS
140

160
JURASSIC

FIG. 1. Phyletic topology of the Pomatiopsidae with time given in millions of years (on a log scale) from the
Jurassic to the present. Branching points: 1. Triculine and pomatiopsine lineages established in Gond-
wanaland prior to the breakup of the southern continent. 2. Divergence to form the Jullieniini (left grouping) in
the Miocene. 3. Radiation of specialized Lacunopsis (Lacunopsini), which diverges from the Triculini.
Lacunopsis, on shell characters, resembles marine and freshwater Neritidae. Some species converge on
Anculosa (Pleuroceridae), Littorina (Littorinidae), or Calyptraea (Calyptraeidae). 4. Seven genera evolved in
the Miocene, probably much at the same time. Pachydrobiella (PA) converges on Pachydrobia (PAC) ofthe
Triculini in shell shape and structure. 5. Anatomical and shell data clearly indicate that Hydrorissoia (HY) and
Jullienia (JU) diverged from a common ancestor. 6. A late Miocene radiation took place in Japan, giving rise
to the endemic genera Blanfordia (B) and Fukuia (F), and Cecina (C). Cecina spread to western North
America, while Pomatiopsis (P) occurs only in the U.S.A. 7. Blanfordia and Fukuia have either diverged from
a common ancestor or are the same genus. Data thus far available support the former interpretation.

A. Aquidauania, South America. В. Blanfordia, Japan. С. Cecina, Japan, Manchuria, U.S.A. CO. Coxiella,
Australia. Е. Fukuia, Japan. H. Halewisia, Mekong River. HU. Hubendickia, Mekong River. НУ. Hydroris-
soia, Mekong River. JU. Jullienia, Mekong River. KA. Karelainia, Mekong River. L. Lacunopsis, Mekong
River. O. Oncomelania, China, Japan, Philippines, Sulawesi. P. Pomatiopsis, U.S.A. PA. Pachydrobiella,
Mekong River. PAC. Pachydrobia, Mekong River, PAR. Paraprosothenia, China. Mekong River (Thailand,
Lao). S. Saduniella, Mekong River. T. Tomichia, South Africa. TR. Tricula, India, Burma, China, Philippines,
Mekong River (from Davis, 1979).

DAVIS

212

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POMATIOPSID EVOLUTION 213

The tribes and genera of the Triculinae are
separated by discrete qualitative morphologi-
cal gaps (Davis, 1979, 1980; Davis & Greer,
1980). Some 28 characters are of use in rec-
ognizing these taxa because the taxa have
shared derived states of these characters
and/or uniqueness of certain derived states
(Table 2). Of these characters, 14 are from
the female reproductive system (50%), seven

are from the male reproductive system (25%)
(only one is from the penis), four are shell
characters (14%), two are radular characters
(7%), and one is osphradial (4%).

The Triculinae provide an excellent oppor-
tunity for studying how higher taxa evolve.
The monophyletic assemblage (Davis, 1979)
is large enough to explore how species of vari-
Ous adaptive zones have radiated, and to un-

TABLE 2. A list of 28 characters that are used to recognize tribes and genera of the Triculinae. References to
illustrations or discussions of character-states are given; these are one or more of Davis, 1979, 1980 (=
1980a below); Davis & Greer, 1980 (= 1980b below); Davis et al., 1976.

Shell
1. shape
2. sculpture
3. size
4. thickness

Central tooth
5. anterior cusp morphology
6. size of blade supports

Osphradium
7. length

Female reproductive system
8. gonad morphology
9. coiling of the oviduct posterior to the bursa

copulatrix 7

10. position of the opening of the seminal
receptacle

11. length of seminal receptacle

12. oviduct configuration at the bursa copulatric
region

13. length of the bursa copulatrix relative to
length of pallial oviduct

14. length of duct of the bursa copulatrix

15. position of the pallial oviduct relative to the
columellar muscle.

16. Coiling of the spermathecal duct

17. encapsulation of the spermathecal duct

18. vestibule of the spermathecal duct

19. extension of the spermathecal duct into the
mantle cavity (= sperm uptake organ)

20. position of opening of the spermathecal duct
into the bursa copulatrix complex of organs

21. method by which sperm enter female repro-
ductive system at the posterior end of the
mantle cavity

Male reproductive system

22. gonad morphology

23. position of coiling of the seminal vesicie

24. relative length of the vas deferens (Vd@) be-
tween the gonad and seminal vesicle

25. coiling of the vas deferens posterior to the
penis

26. position where vas deferens leaves the
prostate

27. penis has stylet or papilla

28. status of vas efferens

1979, figs. 28-30; 1980a, fig. 7

1979, figs. 28-30; Table 12; 1980a, fig. 7
1979, figs. 28—30; Table 11; 1980a, fig. 7; Table 6
1979, figs. 28-30; 1980a, fig. 7

1979, fig. 4; 1980a, fig. 6
1979, fig. 4; 1980a, fig. 6

1976, fig. 7

1979, figs. 11-15; 1980a, fig. 11
1980a, figs. 4, 8, 13

1979, figs. 3, 11-18; 1980b, fig. 10
1979, fig. 12

1979, fig. 3

1979, figs. 12, 13
1979, figs. 11-16; 1980a, fig. 13

1979: 107
1979, fig. 12

1980b, fig. 7

1979, fig. 14C; 1980b, fig. 10

1979, fig. 3; 1980a, figs. 8, 13; 1980b, fig. 10

1979, fig. 3; 1980a, figs. 5, 8; 1980b, fig. 10

1979, fig. 19; 1980a, fig. 11; 1980b, fig. 9
1979, figs. 11-15; 1980a, fig. 12

1980a, fig. 12
1979, fig. 12A
1979, figs. 14, 15

1976, fig. 10; 1979, fig. 10; 1980b, fig. 9
1979, figs. 11-15; 1980a, fig. 11; 1980b, fig. 9

rr А ——/С/:/—

214

derstand the directions of morphological
change that permitted the crossing of thresh-
olds of various adaptive zones to new adap-
tive zones.

In the Triculinae, as in other higher taxa, we
see four aspects of adaptive radiation: first
order adaptive radiations, null radiation, sec-
ond order adaptive radiations, and macro-
adaptive radiation.

The term adaptive radiation was first used
by Osborn (1918) and fully exploited by Simp-
son (1949) who stated: “Adaptive radiation is,
descriptively, this often extreme diversification
of a group [e.g. mammalian or reptilian radia-
tion] as it evolves in all the different directions
permitted by its own potentialities and by the
environments it encounters.” Stanley (1979)
stated: “Adaptive radiation is the rapid pro-
liferation of new taxa from a single ancestral
group.” These authors are discussing what |
call here macro-adaptive radiation, a higher
taxon or a higher taxon clade that is, in fact,
recognized as such because of its component
clades. The Triculinae are a macro-adaptive
radiation.

A first order radiation is equated with a
genus, which is a composite of at least two,
but usually more than two species. The en-
trance into a new adaptive zone made possi-

Е. CORONATA L MASSE!

<< OVATE-
Co,
Nic

LACUNOPSINI N

L.SPHAERICA
ah

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saps TRICULINI

DAVIS

ble by a new morphological or physiological
innovation is associated with the rapid prolif-
eration of new species that fill various niche
dimensions. A null radiation is a monotypic
genus, a taxon recognized by the discrete
morphological gap from other genera to which
it is phyletically allied. Such a genus may be
the basis for a first order radiation of the fu-
ture, or represent a dead-end due to the very
nature of the morphological innovation(s) that
distinguishes it. Planispiral Saduniella of the
Triculinae is such a genus. A second order
radiation involves two or more phyletically
allied first order radiations and can be
equated to named taxa between generic and
high taxon clades under discussion. Within
the Triculinae, the tribes Triculini and Julli-
eniini are second order radiations.

Detailed discussions of the evolution of de-
rived character-states and taxa with those
states have been given (Davis, 1979, 1980;
Davis & Greer, 1980). In review, the most pro-
found changes involved the reproductive sys-
tems as the progenitors of the modern Tricu-
linae adapted to the evolving Mekong and
Yangtze River systems. Changes were es-
sentially in two directions involving two
clades, the Lacunopsini and Jullieniini. These
changes show divergence from Tricula, which

| 4 | И > >
Se И.

L. ROLFBRANDTI

yes a

L. FISCHERPIETTI

CALYPTRAEA RADIANS

FIG. 2. Shells of representative species of the Lacunopsini showing diversity in shell shape and showing a
closer relationship of the Lacunopsini to the Triculini than to the Jullieniini (also see Fig. 1). The marine
mesogastropod Calyptraea radians is illustrated to show how similar the species is to L. fischerpietti. These
two species are highly convergent in shape, growth patterns, and sculpture (from Davis, 1979).

POMATIOPSID EVOLUTION 215

has the most generalized character-states.
Many of these derived innovations are corre-
lated with swift-water habitats as has been
shown statistically (Davis, 1979). There is a
lack of species with generalized character-
states adapted to swift-water habitats.

The Lacunopsini (Fig. 2) most likely evolved
from an ancestor that also gave rise to Tricula
bollingi (Davis & Greer, 1980). A single first
order radiation is involved, all in the Mekong
River. The niche dimensions filled are swift-
water habitats on rocks where species differ-
ences are seen in shell shape and sculpture,
and positional relationships in the water col-
umn involving rock slope, depth, rock surface,
degree of current. Shell shapes are astonish-
ing for freshwater hydrobioids as shapes con-

Р. VARIABILIS

H. EXPANSA
HALEWISIA

P BAVAYI
PACHYDROBIA

Ч
2тт

LACUNOPSINI

Т. АРЕВТА

TRICULA

TRICULINI

verge on those of marine Neritidae, Littorini-
dae, and Fossaridae. The most remarkable
changes in the reproductive system are the
loss of the seminal receptacle as seen in
Tricula and the development of several ac-
cessory seminal receptacles, and the degree
to which the pericardium is modified and used
to accommodate sperm during reproduction.
А! species are similar in that the central tooth
is a derived type (Fig. 5) modified for scraping
food from rock.

The Jullieniini (Fig. 4) comprise one of the
most spectacular second order molluscan
radiations ever seen in freshwater. This radia-
tion in the Mekong River has five first order
radiations and two null radiations. We know
too little about the Chinese genera Litho-

Р SPINOSA

JULLIENIINI

FIG. 3. Shells of representative species of the three genera of the Triculini. The implication of this tree-like
configuration is that Pachydrobia has more derived character states than does Tricula, reflected in certain
shell features, e.g. ribs, bosses (odd lump[s] on the shell), and solitary spines. Also implied is the basal
status of Tricula relative to the divergent tribes Lacunopsini and Jullieniini, which have more derived char-
acter states (also see Fig. 1). Note also the increase in size (only L. aperta is drawn at a larger scale, as
indicated by the 5 mm scale bar) in P. variabilis, P. fischeriana, etc., compared with Halewisia and Tricula

(from Davis, 1979).

216 DAVIS

glyphopsis, Delavaya, Fenouilia, and Para-
pyrgula (Table 1) to say anything about them.
Incremental derived changes in the female
reproductive system are in the direction of in-
creasing volume and complexity of the repro-
ductive organs (Davis, 1979, 1980). The
generalized hydrobioid oviduct is thrown into
a 360° complex with the seminal receptacle
and spermathecal duct (Fig. 6). This 360° loop
is small in diameter in the least derived genus
(Karelainia) and increases markedly in di-
ameter in the more derived genera. The
gonad is the generalized pomatiopsid type in
Karelainia and is considerably modified in
morphology in the more derived genera.
Elongation of the seminal receptacle is seen
in only a few species of Hubendickia while
extreme elongation is seen in more derived
genera such as Paraprososthenia, Jullienia,
Hydrorissoia, and Pachydrobiella. Extreme
elongation and recurving or coiling of various
sections of the vas deferens are seen in the
more derived genera and especially pro-
nounced in the most derived genera, Jullienia
and Hydrorissoia.

Increasing complexity in the reproductive
system is associated with exploitation of dif-
fering (even if slight) reproductive strategies.
Increasing bulk and complexity of the repro-
ductive system are associated with the
Mekong River triculine fauna (Davis, 1979).
These species are colonizers and opportunis-
tic species in a river that goes through an an-
nual cycle of rampaging floods during the
monsoon season (June through November)
to relative quiet and shallow flow during the
dry season (December through May). The
floods bring high density-independent mor-
tality because of the distribution of habitats
and the sweeping away of snails from low-
water depositional areas. There are high re-
productive rates in the single short low-water

breeding season available to these annual
species. The relative volume of reproductive
Organs discussed above coupled with the
tremendous biomass of young produced (see
Davis, 1979) attest to comparatively great
amount of energy put toward reproduction
(contrast Pomatiopsinae, Davis, 1979: 69).

Growth and reproductive activities of
Mekong River species are remarkably in
phase with the annual river cycles. Different
groups of species mature, reproduce, and die
at different times once the dry season begins
and water levels begin to drop. All Triculinae
are semelparous as far as is known. Once
Pachydrobia reproduces, the reproductive
system slowly disintegrates. This is first seen
in the male where the penis begins to disinte-
grate; it is later seen in the female where the
ovary and pallial oviduct disintegrate. The
snails live on for a month or more after the
onset of this disintegration process. Once
Tricula aperta has laid its eggs, it dies and
there is a period of about one month when no
adults are seen and no hatched young can be
found.

Additionally, there is a temporal division of
river habitat as regards maturation and repro-
duction. A given habitat may have one group
of species at one period of low water that re-
produce and die, to be replaced by different
species that hatch, grow to maturity, etc.
(Davis, 1979). The temporal division keeps
pace with the annual cycle of habitat emer-
gence. As water levels begin to decrease in
October, habitats begin to emerge and form.
First island masses and the larger waterfalls
appear, followed by smaller islands, embay-
ments between islands, lakes and pools on
islands, smaller rapids, sandbars, and finally
shallow quiet areas allowing for considerable
mud deposition. From mid-October or No-
vember through June most habitats are free

—=>

FIG. 4. Shells of representative species of the seven genera of the Jullieniini grouped to reflect relationships
and a radiation of shell types within each genus. The trend from bottom to top is one of generalized to
specialized both in shell features and anatomy. Spiral and nodulate sculpture is derived. Jullienia is most
specialized in terms of sculptural patterns, large size, and odd shapes (e.g. flattening of the base of the shell
in some species) as well as anatomy. In Hubendickia, the shells, depending on the species, are smooth or
ribbed. Nodes are seen on the adapical ends of the ribs in two species. In Paraprososthenia, shells range
from smoothly ribbed, with solid spiral cords, or with spiral rows of nodes. P. hanseni has morphs ranging
from smooth, one spiral row of nodes to several spiral rows of nodes on the body whorl. Hydrorissoia and
Jullienia are, on the basis of anatomy, phenetically very similar. Together with Paraprososthenia they form
the Jullienia complex. Karelainia parallels Paraprososthenia in shape and sculpture but diverges consider-
ably in anatomy. Note that К. davisi has several morphs. Fossarus foveatus is shown as an example of
convergence between unrelated taxa. F. foveatus is similar to species of Jullienia in shell shape and
sculpture. F. foveatus is in the marine family Fossaridae. All shells are drawn to the same scale except the
six Jullienia with the 5 mm scale bar (from Davis, 1979).

POMATIOPSID EVOLUTION 217

H.GRACILIS sy, ELEGANS

HYDRORISSOIA

FOSSARUS

HUBENDICKIA

JULLIENIINI
TRICULINI

218

from flooding and destruction caused by the
monsoons. Because of the floods, the con-
figurations of sandbars, islands, and rapids
change yearly. A population that flourished in
a muddy depositional area one year may be
buried under stones and cobbles the next
year. Species with the most derived reproduc-
tive systems appear to grow and mature rap-
idly and to reproduce during lowest water.
Taxa with the most generalized systems re-
produce during higher water periods before
and after the four-month lowest-water months
(Davis, 1979).

The foregoing discussion has involved 75%
of the derived characters. Different feeding
habits involve yet another niche dimension
especially exploited in the second order
Jullieniini radiation. This is reflected by the
morphology of the central tooth of the radula
(Fig. 5). The generalized central tooth seen in
the Triculini and all Pomatiopsinae is found
only in a few species of Hubendickia of the
Jullieniini. Species of all other genera have
derived types of teeth. Finally, shell char-
acters reflect adaptations to different micro-
habitats and perhaps to living in sympatry with
different species (Figs. 2-4). Only two or three
species of Hubendickia have the smooth,
ovate-conic, small shell that is the generalized
hydrobioid type (Davis, 1980). Modification of
shell characters from generalized to most
derived follows a parallel course in each of the
two second order and Lacunopsini first order
adaptive radiations of the Triculinae. There is
a net increase in size, and there appears to be
a progression from smooth to ribbed, nodu-
late ribs, reticulate sculpture, spiral noded
cords, and finally odd spines and nodes.

DAVIS

There is another progression from ovate-
conic to diverse symmetric shapes including
planispiral, and finally to asymmetry. In the
Jullieniini the trends in increasing complexity
of the reproductive systems generally parallel
the three trends in shell characters and the
trends in central tooth morphology.

It is in Hubendickia that we have an indica-
tion that certain sculptural character-states
are related to species living in sympatry. We
see a possible case of character displace-
ment. At Khemarat, Thailand five species of
Hubendickia live sympatrically. It is common
to find four species in great numbers (hun-
dreds) in a handful of algae. Each of these
species has a distinctive shell sculpture т-
volving ribs. One of these species was called
H. spiralis Brandt because of pronounced
spiral micro-sculpture. These species crawl
over each other continuously. It seems prob-
able, although it is untested, that sculpture
serves for species recognition for mating pur-
poses. It was determined on the basis of over-
all morphological similarity that H. siamensis
spiralis was a synonym of Н. sulcata (Bavay)
of the lower Mekong River (near Cambodia)
as was also H. siamensis Brandt of the Mun
River that flows into the Mekong River at the
isles of Ban Dan (Davis, 1979). No other spe-
cies of Hubendickia lives in the Mun River
where one finds the population of H. sulcata
referred to by Brandt as H. siamensis. Snails
of this population entirely lack spiral micro-
sculpture. Over 100 miles south of Khemarat
at Khong Island there are more than 50 spe-
cies of Triculinae but few species of Huben-
dickia. Populations of Hubendickia are rarely
sympatric in the sense that they are found

—

FIG. 5. Central teeth of representative species of Triculinae and Pomatiopsinae compared with the central
tooth of Hydrobia totteni. А, В. Stylized drawings showing structures of the central tooth. Note that the blade
(BI, blackened layer) is a layer fused on the dorsal aspect of the blade support (Bsu). The lateral view of the
tooth is shown in B and EE. C-E. Hydrorissoia hospitalis (Triculinae: Jullieniini). F, G. Hubendickia cylind-
rica (Triculinae: Jullieniini). H. Saduniella planispira (Triculinae: Jullieniini). |. Paraprososthenia levayi
(Triculinae: Jullieniini). J-L. Jullienia harmandi (Triculinae: Jullieniini). М. Pachydrobia variabilis (Triculinae:
Triculini). N. Hubendickia coronata (Triculinae: Jullieniini). O-Q. H. gochenouri (Triculinae: Jullieniini). R.H.
polita (Triculinae: Jullieniini). S. H. pellucida (Triculinae: Jullieniini). T. Oncomelania hupensis (Pomatiop-
sidae: Pomatiopsinae). U. Hydrobia totteni (Hydrobiidae: Hydrobiinae). V-Y. Hydrorissoia elegans
(Triculinae: Jullieniini). Z. Lacunopsis conica (Triculinae: Lacunopsini). AA-CC. Halewisia expansa male
(Triculinae: Triculini). DD. Karelainia davisi (Triculinae: Jullieniini). EE. Tricula aperta (Triculinae: Triculini).
FF. Jullienia acuta (Triculinae: Jullieniini). GG. Pachydrobiella brevis (Triculinae: Jullieniini). HH. Halewisia
expansa female (Triculinae: Triculini) All teeth without шт bars are drawn to the same scale as EE. 2 was
drawn at Уз the magnification of EE. Note the multiserrated blade of J-L and GG and the pauciserrated blade
of AA (from Davis, 1979).

Acu, anterior cusp; Bc, basal cusp; BI, blade; Bsu, blade support; Edg, edge of the blade support; Fa, face
of the tooth; L, length of tooth; La, lateral angle; L of Acu, length of anterior cusp (to the Edg); Led, lateral
edge of tooth face.

POMATIOPSID EVOLUTION 219

220 DAVIS

living intermixed on the same substrate in the
same area. Spiral microsculpture is weakly
developed in a few populations of H. sulcata,
found on only some individuals of other popu-
lations, and is entirely lacking from individuais
of yet other populations. It is evident that in
the absence of high incidence of congeneric
sympatry, spiral microsculpture breaks down.

Many shell shapes are clearly interpretable
when one observes how the species live. The
shells of one species converge on the shells
of phyletically totally unrelated groups be-
cause the animals of these different groups
position themselves on various substrates in
the same way. The resemblance of various
Lacunopsis species to marine Littorina has
been discussed in detail elsewhere (Davis,
1979, 1980).

Tricula of the Triculini radiation (Fig. 3) has
the most generalized morphology and is rep-
resented in the Mekong River by only one
species, 7. aperta (Temcharoen). The one
successful Triculini radiation in the Mekong
River involves Pachydrobia. Again, this spe-
cies-rich radiation involves innovations in the
female reproductive system and establish-
ment in a range of habitat types as reflected in
a range of shell morphologies that fit the
trends discussed above.

It is evident that entrance into an adaptive
zone, which permitted a new first order radia-
tion of Triculinae, enabled some species of
that radiation to overlap many niche dimen-
sions of species of other first order radiations.
A single scoop of a hand sieve (500 ml capac-
ity) through a muddy substrate often yields
several thousand snails of eight to ten species
of three to six genera (Davis, 1979). Numer-
ous species in sympatry on a rock or patch of
mud or small area of sandy-mud is the rule,
not the exception. The snails do not seem to
be resource limited unless it is for space for
egg deposition.

A number of species do occupy unique
space. An example is Lacunopsis fischer-
pietti Brandt, the largest triculine in the Me-
kong River (shell diameter of 15 to 18 mm),
which closely resembles the marine species
Calyptraea radians. L. fischerpietti lives one
or two per boulder on the vertical faces of
huge boulders, facing the swiftest current.
Other examples are: Lacunopsis harmandi,
which lives at the interface of swiftly flowing
water and air. Jullienia costata lives crowded
by the thousands, packed shell to shell, on
vertical cliff walls in rushing waterfalls,
splashed continuously by the spray. Some
populations of Hubendickia polita are nearly

amphibious, living on damp rock just above
the water line. Lacunopsis massei lives with
no other species, each individual is separated
by at least 15 mm from other individuals on a
polished smooth horizontal rock surface over
which a strong current runs and the water is at
least one meter deep. Several species of
Pachydrobia live allopatrically in sandbars
where few or no other species live.

Tempo and mode of triculine evolution

Given the time period for the Himalayan
orogeny, initiation of the river drainage sys-
tems involved, and the presence of fresh-
water sediments in the critical region of north-
ern Burma, it is reasonable to estimate the
age of the modern triculine radiation as start-
ing about 10 to 12 million years ago at the
longest (Davis, 1979, 1980). Following the
arguments of Stanley (1975, 1979) | calculate
R, the fractional increase of species per unit
time using the equation № = N.eft, which is
equivalent to В = (1nN)/t. № is the original
number of species (= 1 considering that the
Triculinae are monophyletic and a single suc-
cessful introduction from the Indian Plate is all
that was needed to produce the macro-radia-
tion fanning out along the three aforemen-
tioned arcs); N is the number of species now
living, t is the time, e is the base of the natural
logarithm. For the Asian Triculinae as a whole
А = 0.40 to 0.48 (My-1) depending on t of
12 or 10 million years ago. This rate is ex-
tremely great and exceeds that of the mam-
malian Muridae that have evolved over 19 mil-
lions years (R = 0.35). R for the Triculinae is
several times greater than for any other mol-
luscan group known (А = about 0.067 My-1
for several families of marine gastropods; R =
0.046 — 0.087 My-1 for several families of
marine bivalves; see Stanley, 1979). If we
calculate R for two second order radiations
and major primary radiation we see the follow-
ing result: Triculini, В = 0.31 My-1; Lacunop-
sini, В = 0.23 Му-1; Jullieniini, R = 0.35 Му- 1.

This explosive monophyletic macro-radia-
tion is coincident with the massive, abrupt,
and recent tectonics of the Himalayan
orogeny. The strong positive association be-
tween tectonic events, bursts of speciation
and cladogenesis, endemism have been re-
viewed (Taylor, 1966; Davis, 1979, 1980).
Rapidly shifting selective pressures and new
pressures are in evidence as seen in the geo-
logical and geographically distributed after-
math of the processes forming the modern
river drainage patterns of the Irrawaddy,

POMATIOPSID EVOLUTION 221

Salween, Mekong and Yangize rivers. One
sees in the now empty ancient river beds and
dead or drying lake basins of northwestern
Thailand, Laos, and northern Burma how
tectonic changes created new aquatic sys-
tems only to surrender these to new stream
captures, new lake formations leaving behind
isolated lakes or empty basins. We see in the
transient aquatic world at the eastern end of
the Himalayan orogeny, over the past 12 mil-
lion years, the elements needed for rapid evo-
lutionary change, the subdivision of popula-
tion into small, isolated, peripheral units
(Wright, 1940). Eldredge & Gould (1972) and
Gould & Eldredge (1977) argue that evolution
proceeded more by rapid and episodic events
of speciation in such peripheral populations
than by gradual change, a theme elaborated
on by Stanley (1979). We see the rapid ap-
pearance of two secondary radiations and a
number of primary radiations that are sepa-
rated from each other by discrete morphologi-
cal gaps. Given the abundance of species
that exist and the recentness of the radiation
we do not see continuous series of morpho-
logical change in transition from one primary
radiation to another. We do not see any sem-
blance of gradual change. The macro-adap-
tive radiation of the Triculinae represents an
excellent case of the punctuational model as
defined by the above authors.

The problem with involving punctuated
equilibrium is one of scale. How much can be
resolved in the fossil record over slices of time
involving one million years when new species
can arise in thousands of years? Paleontolo-
gists do not have the relevant data (Smith,
1981). However, data from Drosophila ге-
search reviewed by Jones (1981) clearly in-
dicate that some populations have sufficient
hidden genetic variation to enable instant
speciation under certain conditions, which
can involve morphological and behavioral
characteristics as well as reductive isolation.
These conditions apparently involve organ-
isms that disperse easily, have relatively short
generation times, and live under conditions
where new ecological space opens. These
conditions apply to the triculine radiation and
are persuasive in considering the triculines as
fitting a punctuational model.

The Pomatiopsinae and the Tomichia
radiation: Introduction

The general features of the pomatiopsine
macro-adaptive radiation have been present-
ed (Davis, 1979). There are eight genera:

Aquidauania, Brazil, South America;
Tomichia, South Africa; Coxiella, Australia;
Oncomelania, Asia; Blanfordia and Fukuia,
Japan; Cecina, Japan, Manchuria, western
U.S.A.; Pomatiopsis, U.S.A. Unlike the
Triculinae, various pomatiopsine taxa are
amphibious, saltwater tolerant, terrestrial and
arboreal in addition to being freshwater aquat-
ic. The relictual vicariant distributions о!
Tomichia, Coxiella, and Aquidauania are
consistent with a Gondwanaland origin, espe-
cially as these genera are more closely relat-
ed to each other (in terms of overall morpho-
logical similarity) than any one of them is to
the more derived Oncomelania. Oncomelania
has а distribution from northern Burma
(Pliocene-Pleistocene fossil) to Japan with an
arc following the Yangtze River, through
Taiwan, to the Philippines and Sulawesi
(Davis, 1979, 1980).

| Knew from preliminary dissections of
Tomichia ventricosa sent to me at the Univer-
sity of Michigan, Ann Arbor, Michigan, U.S.A.,
in 1964 that this species was a member of the
Pomatiopsinae. Connolly (1939) listed 10
species of Tomichia from South Africa but
said nothing about their soft parts, morphol-
ogy or ecology. On the basis of shell and
radula data presented by Connolly (1939), |
saw a resemblance between Tomichia dif-
ferens, T. natalensis, and T. cawstoni and
various species of Tricula. | thought that these
species might, in fact, be species of Tricula.
Accordingly, | initiated studies in South Africa
in 1977 to 1) see if one or all of the three
species in question were Tricula, thus
strengthening the hypothesis of South Central
Gondwanian origin of the Triculinae; 2) as-
sess the extent of morphological divergence
among species of Tomichia and Tricula that |
might find there; 3) assess the extent of the
Tomichia radiation; 4) learn about the ecology
of the relevant species and, if possible, about
the origin and radiation of Tomichia.

Methods of collection and dissection were
those of Davis & Carney (1973) and Davis
(1979). Collections were made from the
Orange River, Namaqualand in the west be-
neath the escarpment along the entire coast of
South Africa eastward to Richard’s Bay near
Mozambique (Appendix 1). All localities where
snails were found are shown in Figs. 7, 8.
Anatomical data and systematic analyses are
given in Appendix 2. Types examined are dis-
cussed in Appendix 3. As a result of these
data | have reduced the number of species of
Tomichia in South Africa to seven (Table 3).
The shells and distribution of these species

222 DAVIS

FIG. 6. Female reproductive system. The generalized character states are seen in the box: A, Hydrobiidae;
B. Tricula burchi, Tricula aperta; C, Tricula bollingi. D, Pomatiopsinae. E, Derived oviduct circle complex of
the Jullieniini. The short seminal receptacle of Hubendickia (Sr-Hub) is considered generalized; the elongate
one (Sr), derived. F, Karelainia; a very condensed oviduct circle complex with short Sr.

Abbreviations: Apo, anterior pallial oviduct; Bu, bursa copulatrix; Cov, Coiled section of oviduct; Csd,
common sperm duct; Dbu, duct of the bursa; Dsr, duct of the seminal receptacle; Emc, posterior end of the
mantle cavity; Oov, opening of oviduct to Ppo; Ov, oviduct; Ppo, posterior pallial oviduct; Sd, spermathecal
duct; Sdu, sperm duct; Sr, seminal receptacle; Sr-Hub, seminal receptacle of Hubendickia; Vc, ciliated

ventral channel (from Davis, 1980).

are shown in Figs. 7 and 8. T. cawstoni is
possibly extinct (see Appendix 3). Т.
alabastrina (Morelet) listed by Connolly
(1939) is not a species of Tomichia but of
Hydrobia s.s. (Davis, in prep.).

Morphological species concepts
Few morphological differences serve to

separate the species (Appendix 2, Tables 4—
6). T. natalensis and T. differens are unques-

tionably species of Tomichia. Those differ-
ences that do occur among species are pri-
marily quantitative. The only morphological
differences seen among species involve shell
shape, size, tendency for shell micro-
sculpture, position of the tip of the radular sac,
very slight differences of point of entry of the
spermathecal duct into the bursa copulatrix
and slightly different positional relationship
between the openings of the sperm duct and
spermathecal duct into the bursa copulatrix.

223

POMATIOPSID EVOLUTION

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POMATIOPSID EVOLUTION 225

TABLE 3. South African species of Tomichia Benson, 1851.

Type-species: Truncatella ventricosa Reeve, 1842: 94, pl. 182, fig. 2, by monotypy.
Type-locality: South Africa, marshes of the Cape Flats.
Distribution of type-species: South Africa, coastal regions below the escarpment from Ysterfontein to
Agulhas, Cape Province.
Species of Tomichia (+ = synonyms)
1. Т. cawstoni Connolly, 1939. Kokstad, Cape Province
2. T. differens Connolly, 1939. Die Kelders, on coast of Walker Bay, about 10 mi. S of Stanford, Cape
Province
3. T. natalensis Connolly, 1939. Lower Umkomaas, Natal Province
4. T. rogersi (Connolly, 1929). Stinkfontein, Namaqualand
Hydrobia rogersi Connolly, 1929
T. tristis (Morelet, 1889). Port Elizabeth, Cape Province
Hydrobia tristis Morelet, 1889
+ T. lirata (Turton, 1932). Port Alfred, Cape Province
Assiminea lirata Turton, 1932
6. T. ventricosa (Reeve, 1942)
+T. producta Connolly, 1929. Eerster River, Cape Flats, Cape Province
7. Т. zwellendamensis (Kuster, 1852). Lakes and streams in Zoetendol Valley, Bredarsdorp District,
Cape Province
Paludina zwellendamensis Kuster, 1952: 53, pl. 10, figs. 19-20.

TABLE 4. Comparison of Tomichia species using 25 characters and their states. There is at least one
difference among the species involving each character. Characters 18 to 24 involve scaling (see Table 6).
In a two state character 0 = no; 1 = yes. МС, no data.

Characters and character states T.d. T.n. Tr TEE T.v. Tez

1. Shell length based on length of last three whorls
(see Fig. 12). 0 0 2 1 1 0
а. small (0)
b. medium (1)
c. large (2)

2. Shell aperture shape 1 2 0 0 0 0
a. ovate (0)
b. ovate-pyriform (1)
c. subquadrate (2)

3. Shell shape 0 1 2 2 2 2
a. ovate (bullet-shaped) (0)
b. ovate-conic (1)
c. turreted (2)

. Shell peristome brown-rimmed (0, 1)

. Shell peristome complete and well-developed (0, 1)
. Shell columellar twist evident (0, 1)

. Shell outer lip thin (0, 1)

. Shell spiral microsculpture
a. none (0)
b. on some shells (1)
c. commonly seen (2)
d. strong and producing malleations (3)

9. Shell inner lip reflected 0 0 0 1 2 1
a. not so (0)
b. slightly (1)
с. pronounced (2)

ONO B
5 ©) fe) = ©
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(se) (el = ©
je) oY ay MO

226 DAVIS

TABLE 4 (Continued)

Characters and character states Ted:

10. Radula central tooth formula 1
90)

2(3) — (3) 2
11. Radula cusps on outer marginal may be > 11 (0, 1)

12. Radula cusps on inner marginal may be > 13 (0, 1)
13. Tip of radular sac ventral to buccal mass (0, 1)

14. Sexual dimorphism in shell length (0, 1)

(>) (=>) (Se) fee (©)

15. Shells of males and females
a. have same no. whorls (0)
b. males have more (1)
c. females have more (2)

16. Spermathecal duct opens into the bursa: 1
a. posterior end, <.35 mm from end (0)
b. >.40, <.60 mm (1)
© 0 (8)

17. Spermathecal duct opens into left ventrolateral edge
of bursa (0, 1) 0

18. Pleuro-subesophageal connective longer than ex-
pected for body size (0, 1) 0

19. Body length relative to shell length 2
a. longer than expected (0)
b. shorter than expected (1)
с. as expected (2)

20. Length radula/length of buccal mass 2
a. greater than expected (0)
b. less than expected (1)
с. as expected (2)

21. Length of bursa/length of pallial oviduct 2
a. greater than expected (0)
b. less than expected (1)
с. as expected (2)

22. female gonad 1
a. longer than expected (0)
b. shorter than expected (1)
с. as expected (2)

23. Length of pleurosupraesophageal connective 2
a. greater than expected (0)
b. less than expected (1)
с. as expected (2)

24. Gill filaments (male and female) 2
a. more than expected (0)
b. fewer than expected (1)
с. as expected (2)

25. Gill filament no. sexual dimorphism (0,1) 0

D © оо

192

OO = —

POMATIOPSID EVOLUTION 227

There are differences in the number of gill
filaments. A number of quantitative differ-
ences are seen once data are arranged to
permit scaling (Table 6). We do not see the
kind of shell shape and sculptural diversity
that is common among species of various
triculine genera. We do not see any clado-
genesis.

Discussion of relationships

On the basis of the morphological data
(Tables, Appendix 2), 25 characters and their
character states serve to discriminate among
species (Table 4). As seen in Table 5, species

TABLE 5. Number of differences among species of
Tomichia based on data in Table 4.

differ by as few as seven (28%) and as many
as 20 character states (80%). Of these char-
acters, 9 (36%) involve shell characters, 4
(16%) involve radular characters, 3(12%) re-
late to sexual dimorphism (shell, gill filament
number), 2 (8%) are internal anatomical
features involving the bursa copulatrix and 7
(28%) involve scaling (Table 6)—compari-
sons of all species to assess whether or not
the number and/or size of organs/structures
correlate with overall size.

Aside from shell size and shape, the spe-
cies do not differ much from each other. There
are only two qualitative differences of internal
morphology, i.e. clearly seen changes in
structure or position of organs or structures.
These are the position on the bursa where the
spermathecal duct joins the bursa; the posi-
tion on the bursa where the sperm duct joins
the bursa. All other differences are quantita-

ds ee ВЕ tive and the seven character-state differences
T. differens ea a НОА involving scaling necessitated a careful com-
T. natalensis 041 43140) 20 parison of all species for all measurements to
T. rogersi OT 48-522 uncover subtle differences.
T. tristis 17 2 In analyzing data for scaling (Table 6)
T. ventricosa — 11 trends are looked for that clearly deviate from
T. zwellendamensis —

the expected. Expected trends are: 1) a de-

TABLE 6. Species ranked in decreasing shell size based on length of the last three whorls in order to assess
if size or numbers of structures correspond to overall size based on shell size.

Length of
bursa
copulatrix
Length of Length of Length of radula - length of Length of
last three Length of buccal = length of pallial bursa
Species whorls body (9) mass buccal mass oviduct copulatrix
T. rogersi 68-10 ВЫ? ЗЕЕ: ES + 05 1.07 136 = 0:04. 1700.11
Т. tristis БИ ЕЕ О.29 26 ЕЕ 183 = 051 0.95* SEDO ZA
T. ventricosa e OE 012 1.06 Sie 0.072 805
T. differens 43550714208 3=230 42 1.0) O12 1.26* EA E
1.19
Т. zwellendamensis 4.1+0.19 84+08 09+0.2 1.08 29-Е: 041109) 10:23
Т. natalensis Я ЕЕ 228: 200009 = 0/02 0.98 “402101027 1:26} 0:06"

Length of pleuro- No. of gill filaments Length of pleuro-

Length of RPG supraesophageal subesophageal
Ф gonad ratio connective 3 2 connective

T. rogersi 2:26 = 0:3 7:61.06 162 215 DIE 53 Da ait

Т. tristis 200 012 2,61 = 09 .50 = .09 58 56ЕЕЗ Pig ES

Т. ventricosa 1:23 10.3 542.04 .42 + .09 A033, 5558277 .04 + .05

T. differens MOS =10;3° .49'-= 106 30 3207 ЭВЕЕ 372953 .03 + .03

Т. zwellendamensis 1.3 +0.1 .51 + .07 2307 66* Set: .02 = .02

Т. natalensis 1.20 = 0.2 .57+ .04 .36 = .03 30 382," 14 = 07“

*Pronounced departure from the expected trend.
**Sexual dimorphism noted.

228 DAVIS

crease in body length as shell length de-
creased, 2) a correlation of decrease in organ
length with body length decrease, 3) an
optimal size of organ length over a range of
body lengths, 4) the decrease of organ length
with body length until a constraint is reached
where the organ could not function properly at
a smaller size. With regard to the expected
trends we see in Table 6 that buccal mass
length fits the class 3 expectation above and
there is no significant difference among the
four smallest species. On the other hand one
notes, examining columns 3 and 4, that the

fourth smallest species has a ratio of length of
radula divided by length of buccal mass that is
significantly greater than that seen in any
other species, larger or smaller; also, the
smallest species has a much larger ratio of
length of bursa copulatrix divided by length of
pallial oviduct (column 5) than all but the
largest species. Other departures from the
expected are marked in Table 6.

There are no pronounced radular differ-
ences (Figs. 9, 10). There is variability in cen-
tral tooth center cusp width but very little in
cusp number. There are none of the profound

FIG. 9. Scanning electron micrographs of radulae A, B. Tomichia differens (D77-13); C, D. T. natalensis

(D78-212); E, F. T. rogersi (D77-20).

POMATIOPSID EVOLUTION 229

LWM

FIG. 10. Scanning electron micrographs of radulae. A, B. Tomichia tristis (D78-53); C, D. T. ventricosa
(077-16); Е, F. (078-80); С, H. T. zwellendamensis (078-74).

230

differences in structure marking different
modes of feeding as seen in the Hubendickia
or Hydrorissoia radiations (Pomatiopsidae:
Triculinae) in the Mekong River (Davis, 1979:
fig. 4). The variation in cusp number is not
impressive considering the notorious variabil-
ity recorded for pomatiopsine populations or
subspecies of Oncomelania hupensis and
Pomatiopsis lapidaria (Davis & Carney, 1973;
Davis, 1967).

The anterior central cusp of the central
tooth may be narrow and elongate in some
individuals of some populations of 7. ventri-
cosa (Figs. 10E, F). Only one in nine individ-
uals of the V; populations had this morphol-
ogy while 90% of the individuals from V;; had
the narrow cusp. Refer to Connolly (1939: fig.
48) for figures of radulae of taxa considered
species by him. He considered that there
were distinct radular types. | conclude from
this study that variation within one or two
populations of 7. ventricosa encompasses
most of the types considered distinct by
Connolly.

One of Connolly's taxa requires special
comment. 7. producta Connolly was named
with the Eerste River, Cape Flats, Cape Prov-
ince, as type locality. The species differed
from Т. ventricosa by more rounded whorls,
deeper sutures, and tall turreted spires of up to
10 whorls. The anterior central cusp of the
central tooth was very broad contrasting the
narrower cusp seen in 7. ventricosa. Variabil-
ity in cusp diameter has been discussed.
Shells matching Connolly’s figure (1939: fig.
47D) are seen most frequently in pans as de-
fined earlier in this paper. The form is especi-

DAVIS

ally seen in the pans near Zoetendalsvlei. No
data support consideration of this form as a
distinct species; it represents part of the vari-
ability of 7. ventricosa.

Considering the minor differences that do
occur among species it is clear (Table 5) that
T. ventricosa, T. tristis, and T. rogersi have
the greatest similarity, with T. differens clus-
tering close to these three species. 7.
natalensis and T. zwellendamensis are dis-
tinctly divergent from each other and from the
cluster containing the other four species. Т.
zwellendamensis shares more character
states in common with T. ventricosa; T.
natalensis is closest to T. tristis.

Ecology

The greatest differences seen among spe-
cies of Tomichia are physiological differences
not morphological ones. These differences,
summarized in Table 7, are discussed below.

Tomichia ventricosa—This species lives in
the broadest range of environments seen for
any species of Tomichia. The species is found
in shallow rivers (H20, 0%..), coastal wetlands
and estuarine settings with low salinity (4-
8700). T. ventricosa is also found in vleis and
pans where the basin fills with water during
the rainy season and dries out slowly during
the dry season, often becoming totally dry for
varying periods of time, i.e. weeks to months.
With the onset of rain, water in the newly filled
basins has a Salinity (8-10%..); as they dry
out the water becomes increasingly saline (to
> 16070).

The river populations apparently live con-

TABLE 7. Habitat types and salinity measurements from habitats where species of Tomichia were found.

Species of Tomichia

T. cawstoni
T. differens

species extinct?
aquatic

T. natalensis
. rogersi
T. tristis

—

aquatic, amphibious

T. ventricosa
vleis

pans

T. zwellendamensis aquatic in vleis, lakes

Habitat

amphibious, stream banks

Salinity (American
Optical Refractometer)

X, 239... (O47
1 locality, 9.5700), М = 11

stream 07, М = 4
(4-59), N = 2

terrestrial, amphibious; high above shore-
line of aborted estuary

aquatic, amphibious, rivers

lagoon 207, М = 1

(487%), N = 2
X, 34%0, (8-83700),
N=9

(25-327), N = 2

X, 2.69. (0-8%..),
N=5

POMATIOPSID EVOLUTION

tinuously submerged in perennially flowing
water. It is probable that the rivers of Sand-
ме, Muizenberg (077-50) and Kleinrivier
near Hermanus (D7) occasionally do dry up
during periods of severe drought but | saw no
evidence for this. | have collected living speci-
mens of this species in only two rivers.

The situation in temporary standing water
vleis and pans is in stark contrast to that in
perennial rivers. Pans are circular and rain-
filled shallow pools most frequently seen near
the shore behind the foredunes of the Cape
Province, especially near Agulhas and Her-
manus. Vleis are irregularly shaped catch-
ment basins or playa lakes often associated
with streams and small rivers that go dry an-
nually or, in some cases, irregularly. Because
of their proximity to the sea and the evapora-
tive cycle, pans and vleis are saline as evi-
denced by the Salicornia-rich fringing vegeta-
tion. The cycle involving Tomichia ventricosa
is shown by a study of this species at Yster-
fontein Vlei in the Cape Province (refer to
Tables 8, 9). | first visited the ме! on 15 No-
vember 1977 and it was nearly full of water

231

with 127 salinity. Snails were found under
rocks near the edge of the water. Blooms of
coarse-stranded green algae were starting. |
marked the high water point and returned on
30 December 1977 during which time the
water had receded horizontally 26 m and the
salinity had more than doubled. Snails were
found in hundreds per m2 in the shallows, on
the substrate and in algal masses that had
accumulated. The snails did not appear in the
least affected by the salinity approximately
equal to that of the offshore ocean water. |
also took soil-substrate samples (400 cm2) at
intervals between the water and the high-
water mark and found that over 92% of the
Snails found in the samples were living (Table
9).
On the 4th of February, 1978, the water had
receded another 15 т and the salinity was
approximately double that of sea water.
Snails were found concentrated as before.
Out in the Vlei, salt crystals were encrusting
the algal mats exposed to the sun (837) but
the snails were moving about normally. On
shore where the water had retreated, algal

TABLE 8. Record of the drying up of Ysterfontein Ме! (V,, 077-11) and the associated increase in salinity.

Date Meters from first highwater marker to edge of water Salinity (7.0)
15 November 1977 0 12
30 December 1977 26 , 28
4 February 1978 41 (edge Н20) 58
91 (out in shallow H,O) 83
March 1978 >.8 km >160
April 1978 >.8 km >160

TABLE 9. Snails, living and dead, sorted from small substrate samples (soil to 2”, grass, Salicornia spp.,
rocks) taken from three localities along a transect from the 15 November 1977 high water mark to the edge of
the water, 26 m away at Ysterfontein Vlei; see Table 8; 30 December 1977.

7.3 т (from high water mark)

Size class (mm)* Living
<1.84 4
1.84-1.96 14
2.00-2.20 25
2.24-2.44 30
2.48-2.68 15
2.72-2.92 12
2.96-3.16** 1
>3.20 1
102

% living 92.7

16.5m 21m
Dead Lx D (LS D
0 20 0 26 0
1 16 0 15 1
1 13 1 33 0
1 18 2 25 0
0 16 0 21 0
2 12 0 12 1
0 3 0 2 0
3 2 0 2 0
8 100 3 124 2

97.1 98.4

“length of body whorl

“*size class for X of mature males and females used for anatomical studies: Appendix 2, Table 12.

232 DAVIS

masses had settled on the Salicornia and
Arthrocnemum plants forming a continuous
thick, tough, dry roof separated from the sub-
strate by 3 to 8 cm. Upon cutting open a hole
in the algal-mat roof one could see active
snails on the moist substrate below. The
snails were amphibious in this humid, moist
environment.

| also watched the drying up of the Vermont
Pan near Hermanus. As long as there was
water in the pan, snails were seen crawling
about on the compressed sandy substrate;
there were hundreds per m2. There was little
fringing Salicornia and/or Arthrocnemum
and no masses of algae in the water. When
the pan was dry and sunbaked, the edge of
the pan was ringed with windrows of dead
Tomichia ventricosa shells. Upon pulling up
rocks and digging down along fissure-like
cracks | collected snails that, upon being
placed in water, were found to be living. It was
thus evident that snails could survive by bur-
rowing below the surface to areas harboring
some moisture, and survive there in estivation
until the next rain.

In yet another pan near Agulhas, the sub-
strate was packed sand and the water level
was nowhere greater than 15 to 20 cm deep.
The salinity was 257 and snails were of ap-
proximately the same density on the substrate
as in the Vermont Pan. The banks of the pan
were packed sand and at the high water mark
were windrows of dead snails with some piles
20 to 30cm deep with thousands of T.
ventricosa shells.

No other snails are capable of living in the
vleis and pans inhabited by T. ventricosa. Т.
ventricosa that survive the period of desicca-
tion emerge during the rainy period into an
environment filling with freshwater where
salinity levels probably reach 9 to 10%... It is
most likely that at this time they reproduce
with exceptionally high intrinsic rate of natural
increase (r). With the dry season the snails
adjust to dwindling water and increasing salin-
ity until they are forced into an amphibious
mode of existence or into estivation. Snails
not reaching safety within the moist chambers
provided by Salicornia plants and algal-mat
roofs or beneath rock piles or other subter-
ranean refuges die due to stranding and
desiccation or by osmotic death when the re-
maining pools of water reach a salinity of 130
to 1607. (as in Ysterfontein Vlei, March and
April, 1978; see Table 8). |

Tomichia ventricosa has adapted to the
greatest range of environmental conditions

and stresses of any species of snail | know:
freshwater, brackish to hyper-saline, amphibi-
ous, dry substrate estivation.

T. differens—This species is found living in
streams and small rivers with perennial water.
At the type-locality this species lives on rocks,
feeding on algae and algal-associated mate-
rial under a thin sheet of continuously flowing
water (5 mm to 3 cm depth). The stream is an
outflow from a limestone cave, some 5 to 6 m
above sea level; the distance from the cave
opening to the sea is some 20 to 25 т. The
species is common along the base of aquatic
sedges in the Nuwejaarsrivier (River) flowing
into Soetendalsviei, a large lake near
Agulhas. In other areas (Appendix 1, D11)
this species is common in and on algal mats
in а small stream. At one locality (Appendix 1,
D4) near Soentendalsvlei, the species was
common in a small stream on 1 January 1978,
the stream had dried up but the snails were
alive under stones and rocks. This stream
flows into the Nuwejaarsrivier and on 19
January 1978, this species was still common
in this river and water levels in the river were
only slightly lowered from levels seen on 1
January 1978.

The salinity of the water was 0 to 47. in 10
of 11 habitats tested; 9.57. in only one habi-
tat (Table 7; Appendix 1). | consider T. dif-
ferens to be a freshwater aquatic species liv-
ing in perennially flowing waters. It probably
has some capability for withstanding desicca-
tion for a limited period of time.

T. natalensis—This species is only found in
Natal; it is primarily amphibious on stream
banks with mud slopes of 45° or less and in
considerably shady and humid environments
provided by grassy vegetation. The habitat is
a cross between that seen for Pomatiopsis
lapidaria and P. cincinnatiensis of the eastern
United States (Van der Schalie & Dundee,
1955, 1956; Van der Schalie & Getz, 1962,
1963). In one location (Appendix 1, N3) snails
were exceedingly numerous among and
under stacks of soggy reeds; many of the
snails were obviously living submerged while
others were out of water. The water always
had 0%. salinity.

This species was only found in the Zululand
region of Natal. Widespread sugar cane farm-
ing in upland and coastal Natal has had a
profound negative impact on streams there.
The few remaining habitats of 7. natalensis
are, in fact, bounded by cane fields and their
future is insecure.

T. rogersi—This, the largest species of

POMATIOPSID EVOLUTION 233

Tomichia, is found in only two localities, isolat-
ed from each other in the high desert of Nama-
qualand. The species is freshwater-aquatic
with some tendency towards being amphibi-
ous. In Lekkersing, a tiny community of human
desert dwellers, this species is located in a
blind canyon with only a single small spring for
water. The spring was capped with a stone
base and windmill. From the base of the wind-
mill, a tiny trickle of water has resulted in a
seepage channel some 23 m long that ends in
sand. The seepage supports a narrow grassy
strip about 0.6 m on each side. The soil is only
damp as there is insufficient water to maintain
any visible surface flow. Snails are numerous
among and under rocks and among the basal
grass stems along the seepage channel.

The habitat at Eksteenfontein, the second
locality, is rather similar except that the spring
is larger and the flow of water produces a visi-
ble stream. Where the water flows through
coarse grass, snails are abundant at the
stems of the grass at the mud-emergent grass
interface just at water level, not submerged in
water.

A search of remaining isolated springs in
Namaqualand, e.g. Khubus (28° 28’ S.; 17°
00’ Е.) or Annisfontein (28° 25’ S.; 16° 53’ Е.)
either yielded no snails or only the pulmonate
Bulinus.

T. tristis—I consider this species to be ter-
restrial-amphibious. | found the species in
only one locality (Appendix 1, T), along the
west bank of the large lagoon at Aston Beach,
Cape Province. The bank was near the junc-
tion of Seekoeirivier (River) and the lagoon,
and close to human habitation. The snails
were not in a marshy area, but high up on the
shore, in a well drained area next to the
mowed lawn of the residence. The snails
were on black loam beneath branches, logs
and piles of similar debris along with a spe-
cies of Assiminea. The habitat was moist and
humid but not wet. It was evident on the basis
of a healthy terrestrial environment that this
locality was only rarely flooded. The snails
were numerous, reaching hundreds per m2
but patchy, being found only under trash,
brush or logs. Water of the lagoon some
meters away was 20%... There were no snails
of any kind among the Salicornia plants at
waters edge or in the lagoon.

T. zwellendamensis—This species is fresh-
water-aquatic living on stems of sedges or on
the bottom of lakes and ponds, not in fast
flowing water, of the Agulhas area. The spe-
cies is particularly abundant near the opening

into Soetendalsviei and in De Hoopvlei, a
large lake along the road from Aguihas to
Potbergsrivier (Appendix 1, 25). In the Hoop-
vlei, snails were hundreds per m2 on the тап-
sandy bottom and algal patches. They live in
permanent lakes or ponds of water with 0 to
87 Salinity (Table 7).

Sympatric Species

| have found sympatry in only two localties
involving three species: T. differens, T. zwel-
lendamensis, and T. veñtricosa. T. differens
and T. zwellendamensis were found in a pan
next to the Nuwejaarsrivier just before the
river emptied into Soetendalsvlei (Appendix |,
D6, Z3). The depth of water in the pan was
5 ст, the bottom was of тай and the water
rather muddy (not due to any recent rain). The
edge of the pan was some 3 m from the river.
T. zwellendamensis was common in grass on
the bottom. There was an occasional T. dif-
ferens among them. T. differens was common
in the river on the stems of rushes and sedges
while there were very few T. zwellendamensis
in that habitat.

The other locality showing sympatry was a
few miles from Soetendalsviei, i.e. Longepan
(Appendix 1, V17; 24). Т. ventricosa was com-
mon in the тат part of the ме, both on
sedges and the sandy bottom. 7. zwellen-
damensis was located where the vlei exited,
flowing to the east, on the stems of reeds in
quiet water. The salinity of the water in the ме!
was 870.

DISCUSSION

In this section | discuss 1) the proposition
that no concrete evidence supports the origin
of Tricula on the African plate, 2) the age and
distribution of Tomichia in South Africa, 3) the
effects of changing environment on Tomichia,
4) preadaptive features in Pomatiopsinae for
an amphibious or terrestrial existence, and 5)
the tempos and mode of pomatiopsine evolu-
tion.

African Tomichia and the Tricula question

There are three species considered to be
Tomichia that occur in central Africa (Brown,
1980). Verdcourt (1951) placed his Hydrobia
hendrickxi from Kakonde, E. Zaire, in the
genus Tomichia because of the morphology
of the central tooth of the radula. Tomichia

234 DAVIS

was characterized by a peculiar raised basal
projection of the central tooth giving the im-
pression of a transverse line across the face
of the tooth (Connolly, 1939; Verdcourt,
1951). The natural affinities of these central
African taxa, removed some 2000 miles from
the South African radiation, cannot be clari-
fied without a thorough anatomical study. In
attempts to learn more about the evolution of
Tomichia it will be essential to study these
taxa in detail to learn if they are, in fact,
Tomichia, and to determine the degree of
morphological relationships to South African
Tomichia.

The transverse bar across the face of the
central tooth is clearly illustrated in Connolly
(1939) and by Davis (1968) in describing new
species of Tricula from northwestern Thai-
land. On the basis of this basal bar and shell
morphology it seemed certain that at least
Tomichia cawstoni, T. natalensis, or T. dif-
ferens would be, in fact, members of the tribe
Triculini (Davis, 1979). On the basis of the
anatomical data this is clearly not the case.
The shells and radulae of certain Tricula and
the above named species of Tomichia are
extremely similar yet they belong in different
subfamilies given their overall morphology.
Accordingly, the relationship of Hydrobia
hendrickxi to various pomatiopsid taxa is
quite uncertain. Shell and radula alone are
not sufficient for assessing relationships.

The so-called basal bar on the central tooth
is a weak and uncertain character. The SEM
pictures of the central tooth (Figs. 9, 10) do
not reveal such a structure. Reexamining
these radulae with transmitted light micro-
scopy reveals the line but at a focal plane
beneath the surface of the face of the tooth.
Thus there is no pronounced ridge on the face
of the tooth; the line is a subsurface structure.
What is characteristic of the Tomichia central
tooth is the extreme development of the inner
pair of basal cusps that swell out far above the
face of the tooth (well illustrated in Fig. 10B).
So great is the outgrowth of these basal cusps
that they often appear connected by a ridge
(Fig. 10H), but this ridge is not in the same
place as the illustrated basal line (Connolly,
1939). Another prominent feature of the
Tomichia central tooth is the deep cavity be-
neath the basal cusps bounded by the lateral
angle (see Fig. 10D or H).

There is no evidence substantiating the
hypothesis (Davis, 1979) that there are
Triculini in Africa. The amazing similarity in
shell and radula discussed above among cer-

tain species of Tomichia and Tricula may re-
flect a common ancestry in the Cretaceous
but no morphologically defined Triculini have
been found in Africa to substantiate this con-
tention. The similarity could just as well reflect
ecology. This weakens the hypothesis that
the Triculinae and Pomatiopsinae diverged
from a common ancester but does not, in light
of other morphological characters and their
history as hosts of parasites compel one to
reject a common ancestor.

Age, modern distribution, man and
the Tomichia radiation

The present coastal configuration of south-
ern Africa was established by the end of the
Cretaceous (Tankard et al., 1981). The fossil
record of the Upper Cretaceous of South
Africa and northern India reveals the pres-
ence of freshwater hydrobioid snails that
were, with high probability, precursors of
modern Pomatiopsidae (Davis, 1979). At that
time when we first can track early Pomatiop-
sidae, they are freshwater-aquatic. The earli-
est record we have of the modern Tomichia
radiation is from the Pliocene, in particular
from Varswater Formation of Langebaanweg
(west of Ysterfontein Vlei, Cape Province)
(Kensley, 1977). Of particular interest are the
freshwater species among the 20 gastropod,
2 bivalve and 1 chiton species found.
Tomichia ventricosa was found with the fresh-
water limpet Burnupia capensis (Walker), the
discoidal planorbid Ceratophallus natalensis
(Krauss), and the spired planorbid Bulinus cf.
tropicus (Krauss). The shells of T. ventricosa
were fragmented (possibly implying transport)
while the fragile planorbids and limpet shells
were beautifully preserved.

There was a marine transgression in the
Pliocene. There is evidence for freshwater
and estuarine environments behind dunes
(Tankard, 1975; Tankard et al., 1981). The
juxtaposition of marine, estuarine, and fresh-
water species indicates an environment simi-
lar to that seen today along the Cape Prov-
ince coast, e.g., the Hermanus estuary. Evi-
dently, a river flowed into a lagoon, which
opened to the sea. Quiet freshwater pond-like
areas adjacent to and connected with the river
would provide a habitat suitable for the
planorbids. There are also numerous remains
of the aquatic plant Chara that suggest such a
habitat. Tomichia would perhaps have lived
as seen today in the river flowing into the
Hermanus lagoon (Appendix 1, 7, 077-29).

POMATIOPSID EVOLUTION 235

These data strengthen the hypothesis that the
modern Tomichia radiation began with fresh-
water snails in a perennial freshwater environ-
ment.

There are to my knowledge no fossils of
other Miocene to post Miocene species of
Tomichia of South Africa. The modern physio-
logical radiation probably evolved starting in
the Pliocene with the full establishment of
aridity in western South Africa and the effects
of aridity spreading eastward.

Two major factors besides aridity apparent-
ly affect the distribution of Tomichia in South

frica: calcium availability and man. The dis-
tribution of calcretes in South Africa are
shown in Fig. 11 as adapted from Netterberg
(1971). A calcrete is a material formed by
calcium carbonate deposited from soil water.
Areas that show absence of calcification are
marked on the map. Tomichia is limited to the
narrow coastal strip associated with the short
drainage systems beneath the escarpments
above which are desert or semi-desert condi-
tions. Tomichia is not found in areas that are
calcium deficient (compare Figs. 7, 8, and
14):

Of particular interest is the area between
the Hoopvlei and Jeffrey’s Вау (21° 30’ to 24°
30’ E. longitude). This strip of coast includes
the Knysna-Wilderness lakes. Initially, | ex-
pected to find Tomichia here because there

28°
ALEXANDER

BAY

CAPE TOWN

AGULHAS

was an abundance of perennial freshwater in-
volving lakes and streams connecting lakes.
These lakes and rivers are, from west to east,
Touwsrivier (= Touws River) emptying at
Wilderness (salinity 4%.) Island Lake (=
Eilandvlei) (7%..), Longvlei (107.0), Rondevlei
(16%); then draining to the east Swartsvlei
(13%), Groenvlei (3%). The Karatararivier
(River) flowing into Ruigtevlei that in turn
flows into Swartsvlei had a salinity of 17... No
Tomichia were found; a limpet was found in
Groenvlei and numerous Hydrobia were
found in Swartsvlei. No gastropods were
found in any of the lakes or rivers except
those mentioned.

The history of these lakes relates to fluctu-
ations of land and sea level from the upper
Pleistocene with a major marine transgres-
sion within the past 7,000 years. During peri-
ods of low sea level, the lakes were probably
dry; the Recent lakes were probably formed
by reflooding (Martin, 1962). In summary,
calcium deficiency and the Recent history in-
volving marine transgression in a series of
basins originating in the upper Pleistocene
are sufficient to explain the absence of
Tomichia. Tomichia sp. recorded from the
Pleistocene fossil deposits on terraces above
the present lakes (Martin, 1962) are undoubt-
edly Hydrobia.

Man has had a profound influence on the

GINGINDLOVU
Y DURBAN

м а

ern

26° 28 930 Sine За 36 38 40°

FIG. 11. Distribution of calcium deposits in South Africa. The shaded areas lack calcium deposits or

calcretes (adapted from Netterberg, 1971).

236 DAVIS

distribution of Tomichia. Species of this genus
are extremely sensitive to changes in their
ecosystems relative to pollution of all types as
well as interferences in the natural dry-wet
seasonal cycles.

Only dead shells of Tomichia are now to be
found in classic sites of Kuils River (34° 01’
S.; 18° 39’ E., near Cape Town Airport), Wild
Bird Vlei, Cape Peninsula (34° 08’ S.; 18° 21’
E.), Kommetiie Vlei (34° 09’ S.; 18° 20’ E.),
Reitvlei (33° 30’ S.; 18° 30’E.). We found ex-
tensive evidence for organic pollution in Kuils
River. In Wild Bird Vlei, a sewage plant now
makes use of the limited available freshwater.
Where there once was a healthy ecosystem,
one now finds a series of hypersaline ponds
of about Уз normal volume (judged on the
basis of the obvious basin that was filled a few
years ago) with salinity >150°%/.., stinking
black mud, numerous dead fish. Kommetjie
Vlei has been drained off; Reitvlei was
dredged out some years ago to supply fill to
make the docks at Cape Town. Instead of a
shallow Ме! there is a large, deep artificial pit.
Numerous subfossil shells are found on the
northern shore above the high water line.

Environment and the modern Tomichia
radiation

We see today in the Agulhas region of
Cape Province, South Africa, what was com-
mon throughout South Africa in the Eocene
into the Miocene, i.e. an abundance of peren-
nial freshwater. | assume, on the available
evidence, that proto-Tomichia of the Eocene
was aquatic, abundant, and widespread. In
the one area of South Africa where there is
still an abundance of freshwater, i.e. the
Agulhas area, there are numerous lakes,
streams, and ponds and rivers of low salinity,
but of suitable alkalinity for hydrobioid snail
life. It is here that one finds the greatest con-
centration of snail-rich habitats and species,
two of which are freshwater-aquatic in per-
ennial systems with salinity <9°/..; mostly
0-5/0.

К is evident that the Tomichia radiation
is species poor compared with the South-
east Asian Triculinae radiations involving
Hubendickia, Pachydrobia, etc. The Tomi-
chia radiation is а physiological-ecological
radiation, not one characterized by morpho-
logical changes. What accounts for this radi-
ation?

The most plausible explanation is the pro-
gressive desertification in South Africa since

the late Eocene, some 39 million years ago
when temperate rain forests in Namaqualand
became depleted and replaced by mixed
sclerophyllic vegetation (Axelrod & Raven,
1978). There has been progressive climatic
change. There has not been a history of
tectonic change in the Cenozoic that is asso-
ciated with morphological changes and ex-
plosive speciation events seen elsewhere.

The Mesozoic break-up of Gondwanaland
caused changing patterns of ocean currents
and climatic processes causing progressive
aridity in South Africa. These changes are
related to the history of glaciation at high lati-
tudes, especially Antarctic glaciation
(Tankard et al., 1981). While glaciation in
Antarctica persisted throughout the Oligo-
cene, its present thickness developed about
mid-Miocene and has existed in present con-
dition from the late Miocene (Shackelton &
Kenneth, 1975; Tankard et al., 1981). The
aridity of western South Africa relates to up-
welling of cold water of the Benguela Current
and the origin of a cold Southern Ocean and
thus could not have pre-dated the late Oligo-
cene (Tankard et al., 1981).

In the Miocene, there was a pan-African
vertebrate fauna in Namaqualand, there was
a mosaic of sclerophyllus woodland, grass-
land, and scrub vegetation and summer rain-
fall that persisted throughout the late Tertiary.
The earliest evidence of a modern semi-arid
environment and winter rainfall in the south-
western Cape Province dates to the Pliocene
(5 million years ago) (Tankard, 1978). Full
semi-arid conditions with winter rainfall were
achieved in western South Africa by the end
of the Pliocene or early Pleistocene.

Progressive aridity stretched eastward. The
short coastal rivers from the Orange River to
Agulhas dry up for the most part during the
dry season, or are reduced to very low flow.
The effect on the estuarine section of the
rivers is that currents and wind-driven waves
heap sand across the openings of the rivers
with the result that lagoon-like aborted estu-
aries are formed that range in salinity from
freshwater (< 5%.) to 22 to 327 with some
becoming hypersaline due to evaporation.
How fresh the aborted estuary is depends on
how impermeable the bar is to salt water.
Tomichia is never found in the lagoon section
of aborted estuaries while Hydrobia (Hydro-
biidae) is common there.

In this century, the Agulhas region has
been affected by eastward reaching aridity. In
the summers of 1969 and 1970 certain large

POMATIOPSID EVOLUTION 237

lakes in the Agulhas region dried up for the
first time in 50 years. Farmers stated that the
winter rains filled the lakes which usually had
water all year long. Zoetendalsvlei was dry
throughout a six to seven year drought that
ended about 1973-1974. During the period of
drought there were pools of water in the river
beds, but the vleis were dry, especially during
summer.

It is evident that populations of Tomichia
responded to increasing aridity in different
ways depending on longitudinal gradients of
aridity and general ecological setting. The
changes were from freshwater-aquatic to-
wards greater physiological tolerance to in-
creased Salinity, amphibious, and finally ter-
restrial modes of existence. The climatic
changes were generally gradual with pulses
of severe drought increasing from west to
east. Changes in selective pressures would
likewise be gradual with erratic events of ex-
treme desiccation increasing from west to
east.

What we see in Namaqualand today are
two relict populations where water availability
is so limited that the snails are virtually am-
phibious. Namaqualand at one time had in-
numerable streams with perennial water.
These streams probably had Tomichia. To-
day, two springs represent the last vestige of
these once widespread populations, and their
continued existence is tenuous.

The coastal vleis and pans so common
from Ysterfontein across the Cape Flats to
Agulhas have probably had annual cycles of
drying from the Pliocene onward, a period of
about 5 million years during which T. ventri-
cosa and T. tristis became adjusted to their
Current ecological situations.

As one passes from Cape Province through
the Transkei to Natal Province one passes
into a wetter and tropical zone. It is here that
one finds amphibious T. natalensis. Presum-
ably there was perennial water in Natal
throughout the Cenozoic; it is not known what
caused 7. natalensis to become amphibious.
It is probable that pulses of drought in this
area caused this adaptation.

Pre-adaptation for an amphibious existence

No modern Triculinae are amphibious ог
terrestrial while some Pomatiopsinae have
become amphibious or terrestrial in various
places and at different times. Are there mor-
phological character-states that pomatiopsine
taxa have that are not shared by triculine taxa

and that predate pomatiopsine taxa of am-
phibious life? The answer is yes. The broad
foot that all pomatiopsines have is essential
for the amphibious mode of existence. An-
other feature is the elongated spermathecal
duct extending to the anterior end of the
mantle cavity that surely would facilitate suc-
cessful copulation and sperm transfer out of
water.

There is evidence that genetically and
physiologically at least some pomatiopsines
are pre-adapted to survive under increased
salinities and desiccation. This was evident
during experiments comparing the perennially
aquatic topotype population of Т. differens
with the Ysterfontein Vlei population of T.
ventricosa for survival under different condi-
tions of salinity and desiccation.

In all desiccation experiments 25 adult
snails from each population were placed in
9 cm Petri dishes. There was a dry and humid
set for each species. Filter paper was fitted
inside the lid and kept moist to produce a
humid chamber. Dry chambers had no filter
paper. The filter paper was moistened only to
the extent that snails would not move about in
the chamber. One dry and one humid cham-
ber were removed from each of the sets and
flooded with water from that species’ environ-
ment on days 7, 14, 30, 60, 120, 150. The
percentage of snails living and dead was
determined by observing them for movement
over a 24 hour period following flooding.
There were no replicates to permit an analysis
of variance. The results shown in Table 10
clearly indicate the profound differences be-
tween species as one would predict. Humidity
is an essential feature for prolonged survival
out of water for both species. Although not as

TABLE 10. Percentage of each species of Tomichia
Surviving after different lengths of time in dry and
humid chambers.

Species

T. ventricosa T. differens
Days humid dry humid dry
7 96 100 96 28
14 96 100 92 4
30 96 92 76 0
60 92 60 60 0
90 96 28 40 0
120 88 16 0 0
150 96 8 0 0

238 DAVIS

TABLE 11. Percentage of each species surviving
one month in water of different salinities (7..).

Species
(Not oxygenated)
(Oxygenated)
Salinities 7. ventricosa T. differens T. differens
0 84 100 96
5 96 100 100
10 96 68 100
15 92 68 100
20 80 0 96
25 100 0 100
33 100 0 0
42 84 0 0
50 52 0 0

tolerant of desiccation as T. ventricosa, а sig-
nificant percentage of 7. differens can survive
at least three months without water in humid
areas. No Mekong River triculine can exist
more than a week out of water.

In the salinity experiments a range of salini-
ties was established using water from Yster-
fontein Vlei (50%..) and DieKelders (0%..).
Chambers with 5, 10, 15, 20, 25, 33, 42, and
5070 were established. A number of snails
were gradually acclimated to each salinity by
slowly increasing or decreasing salinities
every day. Finally 25 snails were placed in
each of the eight containers. There were three
sets; two sets were not aerated (one with 7.
ventricosa, one with T. differens), and one set
aerated (with T. differens). T. differens nor-
mally lives in highly oxygenated environ-
ments. Algae were grown in the water for food
and oxygen (under standing water condi-
tions). The water was changed every 4 to 5
days and dead snails were removed daily to
prevent fouling of the water. After 30 days the
percentage of snails living was determined by
noting activity over 24 hours. Results are
shown in Table 11. Again, there is a profound
difference between species as expected.
Oxygenated water clearly improves survival
of 7. differens under high salinity stress but
only up to 25%... Snails could be acclimated
to 337. salinity and be active for two weeks
before withdrawing into their shells and dying
within one month. With oxygenation T. dif-
ferens can probably live for months at 15 to
20700. The point to be made here is that 7.
differens shows considerable salinity and
desiccation tolerances as a freshwater spe-
cies and could probably be selected to live

under conditions somewhat similar to those
where one finds 7. ventricosa.

Tempo and mode of pomatiopsine evolution

There has been no cladogenesis that one
can detect in the southern continental
pomatiopsines. The Coxiella radiation of
Australia is small and parallels the ecological
adjustments seen in Tomichia ventricosa.
The seven modern species of Tomichia of
South Africa seem to have evolved starting in
the mid-Miocene to early Pliocene in re-
sponse to progressive aridity spreading from
west to east. There was no pronounced
tectonism associated with opening of new
ecological space and considerable morpho-
logical diversity as seen in Southeast Asia.
What is seen is more of a gradual adjustment
to changing climate over a period extending
some 25 million years. This gradual adjust-
ment has resulted in a few physiologically de-
fined species that have few morphological dif-
ferences among them.

There are insufficient data to know when,
precisely, the modern Tomichia radiation be-
gan, i.e. the date of origin of that species from
which the seven modern taxa evolved. 7.
ventricosa is found in the Pliocene and pre-
sumably this precursor was present in the
mid-Miocene about 14 million years ago. If
this date is used as a rough estimate for the
origin of the modern Tomichia radiation, then
R = 0.139. Even if an individual speciation
event was rapid, the overall picture over a
period of 2 to 14 million years indicates a
gradual change contrasted with the Triculinae
radiation. It is clear, in contrasting the Mekong
River Triculinae with the South African
Pomatiopsinae, that there are two distinctly
different tempos of evolution.

The mode of speciation of South African
Pomatiopsinae clearly differs from that of the
Mekong River Triculinae. The difference is
one of a physiological radiation with low
morphological diversity versus a radiation in-
volving pronounced morphological diversity
and comparatively narrow range of physio-
logical adjustment. While this is the major as-
pect of mode that | wish to stress, more
should be said of that aspect of mode involv-
ing the paradigms of punctuated equlibrium
and phyletic gradualism. As discussed above,
the Mekong River Triculinae generally fit the
conditions expected in the punctuated equilib-
rium mode of Gould & Eldredge (1977) and
Stanley (1979). South African Tomichia fit the

POMATIOPSID EVOLUTION 239

gradualistic model only in so far that there is
slight, gradual morphological change and if
the species are defined in traditional terms of
morphology and presumed reproductive iso-
lation. However, the physiological radiation
opens a new dimension for consideration in
comparing paradigms. We do not know the
extent to which the physiological changes
may be punctuational in the sense discussed
by Jones (1981) for Drosophila. Given the
scenario of gradual climatic change and the
absence of an adequate fossil record in South
Africa documenting the presence of species
of Tomichia other than that of Т. ventricosa,
one can only assume a gradual change in
genetically controlled physiological toler-
ances.

The mode and tempo of pomatiopsine
radiation in Asia is more similar to that of the
Triculinae. The introduction of proto-Oncome-
lania from the Indian Plate to mainland Asia
was followed by dispersal to Japan and North
America. At the end of the Miocene, there was
a modest adaptive radiation in Japan involv-
ing cladogenesis and speciation (Table 1) as-
sociated with Japanese tectonism at that time
(Davis, 1979). There is considerable morpho-
logical divergence as well as ecological di-
vergence (Davis, 1979, table 2). Cecina is
marine intertidal; Oncomelania minima and
Pomatiopsis binneyi are freshwater-aquatic,
Blanfordia is terrestrial. Considering introduc-
tion into Asia at 12 or 10 million years ago,
and the 16 modern species that have evolved
(including the subspecies of Oncomelania
hupensis), R = 0.23 or 0.28 My-1 for the
Asian pomatiopsine radiation. This is a com-
paratively rapid rate considering any group of
animals, one associated with tectonics and a
series of morphological changes. Therefore, it
is the tempo and mode of environmental
change and the extent of ecological space
and complexity that determines the tempos
and modes of evolution; it is not a matter of
genetic background.

ACKNOWLEDGEMENTS

| acknowledge the immense help and sup-
port of the South African Museum and its
staff, especially Drs. A. Hully and V. White-
head; Drs. A. C. Brown and G. Branch and
Ms. Jean Smits of the Department of Zoology,
Capetown University; Dr. R. Kilburn of the
Natal Museum. Assistance and helpful dis-
cussions were provided by Dr. D. Brown and

staff of the British Museum (Natural History)
and D. A. Tankard, Department of Geosci-
ences, University of Tennessee, Knoxville. |
acknowledge the help and cooperation of the
Zoological Museum of Oxford. | am indebted
to Drs. K. E. Hoagland, J. B. C. Jackson, W.
D. Russell-Hunter, A. Tankard, and D. Wood-
ruff for reading and commenting on this
manuscript. Jean Smits, an honors student of
Capetown University, conducted the physio-
logical experiments. Ms. Lynn Weidensaul
Monarch prepared and analyzed the radulae,
and prepared the figures of shells and maps. |
made the drawings of anatomy but the final
rendering was done by Ms. Mary Fuges.

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APPENDIX 1. Field data for species of
Tomichia collected for this study. The num-
bers (e.g. О.) correspond to sites marked in
Figs. 7 and 8. Coded sequences such as D77-
13 refer to field numbers (D = Davis; 77 =
1977; 13 = 13th collection in 1977).

T. differens

О, 077-13; type-locality; from rocks in
stream flowing from cave at the base
of the cliff in front of the hotel, Die

POMATIOPSID EVOLUTION 241

Kelders; Cape Prov.; 34° 33’ S.; 19°
22’ E. Davis, С. M. and Smits, J.; 19
Nov. 1977; salinity 2°%oo.

D78-83; headwaters of stream flow-
ing into Soetendalsvlei via Southbos’
farm, crosses track between Jacobs-
dam and Bergplass about 6.5 to
7.0 mi. west of Soetendalsvlei;
Саре Prov.; 34° 43’ S.; 19° 51’ Е.
Davis, G. M. and Dichmont, T.; 19
Jan. 1978; salinity 2%.

078-70; small stream with sedges,
Nuwejaarsrivier, 5km. NW of
Elands—drif, opposite Vogelvlei;
Agulhas region, Cape Prov.; 34° 38’
S.; 19° 52’ E. Davis, С. M.; 17 Jan.
1978; salinity ?

D78-2; bridge crossing stream flow-
ing into Soetendalsviei, road from
Agulhas to Elim, 2.5 km. NW of
Soutbos’ farm; Agulhas region, Cape
Prov.; 34° 42’ S.; 19° 56’ E. Davis, G.
M., Hoagland, K. E. and Smits, J.; 1
Jan. 1978; salinity 27.0.

078-78; same as D78-2; stream
dried up, snails alive under stones,
rocks. Davis, G. M. and Dichmont, T.;
19 Jan. 1978.

D78-71; on sedges in Nuwejaars-
rivier, before entering Soetendals-
vlei, opposite Soutbos’ farm; Agulhas
region, Cape Prov.; 34° 43’ S.; 19°
57' E. Davis, С. M. and Dichmont, T.;
18 Jan. 1978; salinity 09».

078-73; in Nuwejaarsrivier and ме!
next to the river at opening of river
into Soetendalsvlei; Agulhas region,
Cape Prov.; 34° 44’ S.; 19° 58’ E.
Davis, G. M. and Dichmont, T.; 18
Jan. 1978; salinity 07.0.

078-79; on rocks and water plants in
Nuwejaarsrivier below the viei, where
road from Agulhas forks to Elim and
Bredarsdorp. In sympatry with
Gyraulus sp.; Agulhas region, Cape
Prov.; 34° 41' S.; 19° 55’ E. Davis, С.
M. and Dichmont, T.; 19 Jan. 1978;
Salinity Ооо.

078-62; on grass, sticks, mud at
stream margins of Karsrivier, about 2
mi. SW of Bredarsdorp-Arniston
road; Cape Prov.; 34° 35’ S.; 20° 00’
E. Davis, G. M. and Dichmont, T.; 16
Jan.1978; salinity 07

D78-6; on grass in roadside pool,
pool about 70’ long x 20’ wide,
ankle deep, road from Malgas to
Heidelberg, 20 km. from Heidelberg;
Cape Prov.; 34° 11’ S.; 20° 46’ E.
Davis, G. M., Hoagland, K. E. and
Smits, J.; 2 Jan. 1978; salinity 370.

D78-7; small streams alongside road
from Malgas to Heidelberg, 18 km.
from Heidelberg, Karringmelksrivier
drainage; Cape Prov.; 34° 09’ S.; 20°
48’ E. Davis, С. M., Hoagland, К. E.
and Smits, J.; 2 Jan. 1978; salinity
3700.

D78-8; large stream, Slangrivier,
where road from Malgas to Heidel-
berg crosses, about 8km. from
Heidelberg. Snails common on algal
mats; Cape Prov.; 34° 08’ S.; 20° 52’
E. Davis, G. M., Hoagland, K. E. and
Smits, J.; 2 Jan. 1978; salinity 9.59.

D78-55A; stream to E of road from
Riversdale to Stillbaai, Riversdale
area, 4km. N of Stillbaai, stream
flows into Kafferkuilsrivier. Snails
numerous on the algae; Cape Prov.;
34° 19’ S.; 21° 24’ E. Davis, G. M,
Hoagland, K. E. and Smits, J.; 8 Jan.
1978; salinity 4/00.

T. natalensis

D78-208; snails amphibious on mud
stream banks, Inyezane River, 2 km.
from Gingindlovu where back road
from Gingindlovu to the shrimp farm
crosses the river; Zululand, Natal
Prov.; 29° 03’ S.; 31° 37’ E. Davis, G.
M.; 4 Sept. 1978; salinity 0%.

D78-207; snails amphibious, distrib-
uted on damp mud slopes of Inye-
zane River, under old reed stems in
shaded areas. Where highway М>
from Gingindlovu to Empangani
crosses the stream, some 6 km. NE
of Gingindlovu; Zululand, Natal
Prov.; 28° 59’ S.; 31° 39’ E. Davis, G.
M.; 4 Sept. 1978; salinity 09.».

D78-212; snails numerous on mud,
stacks of reeds, amphibious. Imbati
River where highway М> crosses be-
tween Emoyeni and Mtunzini; Zulu-
land, Natal Prov.; 28° 57’ S.; 31° 42’
E. Davis, G. M.; 5 Sept. 1978; salinity
0/00.

242

№

DAVIS

078-213; snails amphibious on
banks of Ubati River at N, road
crossing between 078-212 and
Mtunzini turn-off; Zululand, Natal
Prov.; 28° 57’ S.; 31° 43’ E. Davis, G.
M.; 5 Sept. 1978; salinity 0%.

T. rogersi

T. tristis

077-20; type-locality; stream oppo-
site schoolhouse, Eksteenfontein.
Eksteenfontein = Stinkfontein (name
changed from meaning _ stinking
spring to no longer stinking spring).
Beginning of Stinkfontein River flow-
ing to the Orange River; Namaqua-
land; 28° 50’ S.; 17° 14’ E. Davis, G.
M. and Smits, J.; 29 Nov. 1978; salin-
ity 5700.

D77-19; seepage from small capped
(windmill) spring, Lekkersing; Nama-
qualand; 29° 01’ S.; 17° 6’ E. Davis,
С. M., Whitehead, V. and Smits, J.;
29 Nov. 1977; salinity 4°/o.

D78-53; snails amphibious, high
shoreline under branches, logs, with
Assiminea sp., soil dark black loam.
W side of Seekoeirivier, lagoon at
upper end of the lagoon near Aston,
Bay Beach; Cape Prov.; 34° 05’ S.;
24° 53’ E. Davis, G. M., Hoagland, K.
E. and Smits, J.; 6 Jan. 1978; salinity
in lagoon 20%...

Т. ventricosa

D77-11; snails clustered on rocks in
ме, Ysterfontein; Cape Prov.; 33°
2078.18. 10 /EADaViS 6. M:: 15
Nov. 1977; salinity 127.0.

077-51; 30 Dec. 1977; salinity 28°...

078-88; 4 Feb. 1978; salinity 587 at
center of vlei; 83°/.. in shallows.

D78-86; dead shells collected on
northern shore, Rietvlei, Milnerton;
Cape Prov.; 33° 50’ S: 18? 32’ E.
Davis, С. M.; 28 Jan. 1978; salinity
8700.

077-44А; all dead shells in ме, ме!
three quarters of the way from sew-
age plant to Chapmans Bay, Wild
Bird Vlei; Cape Peninsula, Cape
Prov.; 34° 08' S.; 18° 21' E. Davis, С.
M., Hoagland, К. E. and Smits, J.; 29
Dec. 1977; salinity 158°.

Veg

D77-44B; all dead shells in мег, ме!
at point where water goes subter-
ranean near Chapmans Bay; salinity
407.0.

077-44С; Ме! half way between sew-
age plant and Chapmans Bay; salin-
ity 1607.0.

D77-27; Quaternary fossils collected
in central area, Sandvlei, Ladeside
near Muizenberg; Cape Prov.;
34°05’ S.; 18° 28’ E. Davis, G. М.
and Smits, J.; 6 Dec. 1977; salinity
2700.

077-28; same as 077-27, collected
from main lake, no live snails; salinity
4700.

D77-29; in masses of green algae in
small pool to west of small dirt road
that runs between vlei and railroad
tracks, above Marina Dagama,
Muizenberg; Cape Prov.; 34° 06’ S.;
18° 28’ E. Davis, G. M. and Smits, J.;
6 Dec. 1977; salinity 10%.».

D77-50; snails on underside of float-
ing algal masses, Sandvlei, Muizen-
berg; Cape Prov.; 34° 06’ S.; 18° 28’
E. Davis, G. M., Hoagland, K. E. and
Smits, J.; 29 Dec. 1977; salinity 8700.

D77-39; turn off N, at first Kuilsrivier
exit from Cape Town, bridge over
Kuilsrivier, up stream > mile. No live
snails; Саре Prov.; 34° 01’ S.; 18°
39’ E. Davis, G. M. and Hoagland, K.
E.; 28 Dec. 1977; salinity 3700.

D78-87A,B; Bermont, Vermont vlei
next to road between Hawston and
Onrus. Vlei had dried up completely;
Cape: Prov.; 34° 25’, Sx AGP 107
Davis, G. M. and Whitehead, V.; 29
Jan. 1978; salinity 60%...

D77-16; just before Kleinriviersvlei
widens into Hermanus Lagoon, W of
Stanford between Stanford and
Wortelgat; Cape Prov.; 34° 27’ S.;
19° 25’ Е. Davis, G. M. and Smits, J.;
20 Nov. 1977; salinity 4°/oo.

D77-17; Kleinriviers; dead snails un-
der masses of algae; Cape Prov.; 34°
25’ S.; 19° 19’ E. Davis, G. M. and
Smits, J.; 20 Nov. 1977; salinity
22700.

D77-14; dead shells 34 mile up
Boemans River from bridge at shore,
Franskraal; Cape Prov.; 34° 35' S.;

POMATIOPSID EVOLUTION 243

19° 24’ Е. Davis, G. M. and Smits, J.;
19 Nov. 1977; salinity 19%cc.

078-67; ме! 4km. NW of Wiesdrift;
Agulhas Region, Cape Prov.; 34° 40’
S.; 19° 54’ E. Davis, G. M.; 17 Jan.
1978; salinity 1070.

078-69; small, shallow ме! between
Waskraals Ме! and Voélvlei; Agulhas
region, Cape Prov.; 34° 39’ S.; 19°
51' E. Davis, G. M.; 17 Jan. 1978;
salinity ?

D78-82; small vlei between Vitkyk
and Bergplaas farms, just N of
Soetanysberg, 6 mi W of middle of
Soetendalsvlei; Cape Prov.; 34° 42'
S.; 19” 53' E. Davis, G. M. and Dich-
mont, T.; 19 Jan. 1978; salinity ?

D78-81; small vlei in nature reserve
on М side of road from Rhenosterkop
to Asfontein, on S side of Soetendals-
vlei; Cape Prov.; 34° 46’ S.; 19° 54’
E. Davis, G. M. and Dichmont, T.; 19
Jan. 1978; salinity ?

D78-75A; W side of road from
Soetendalsvlei to Springfield, cross-
es stream flowing to salt pan; Cape
Prov.; 34° 44’ S.; 19° 55’ E. Davis, G.
M. and Dichmont, T.; 18 Jan. 1978;
salinity 25%.

D78-75B; dried, twisting channel to
salt pan on E side of road, snails un-
der dried algae mats and rocks;
Salinity ?

D78-80; pan at Rhenosterkop, 4 mi
W of S end of Soetendalsvlei. Snails
numerous on sand and clustered on
stones; Cape Prov.; 34° 46’ S.; 19°
56’ E. Davis, С. M. and Dichmont, T.;
19 Jan. 1978; salinity 327.0.

D78-64; Rondepan, large viei on S
side of road from Bredarsdorp to
Elim, 14km. from Bredarsdorp.
Snails under stones; Cape Prov.; 34°
37' S.; 19° 56’ E. Davis, С. M. and
Dichmont, T.; 16 Jan. 1978; salinity
20%.

D78-65A; Langepan, main part of
vlei. On road from Bredarsdorp to
Elim, 16km. from Bredarsdorp.
Snails on sedges and sandy bottom;
Cape. Prov.; 34° 37’ S.; 19° 54’ Е.
Davis, G. M. and Dichmont, T.; 16
Jan. 1978; salinity 87.0.

Vig

D78-38; Kowie River, Port Alfred;
Cape Prov.; 33° 36’ S.; 26° 53’ E.
Davis, G. M. and Hoagland, K. E.; 5
Jan. 1978; salinity 327.0.

T. zwellendamensis

078-68; Waskraalsvlei, snails оп
stems of sedges; Agulhas region,
Cape Prov.; 34° 40’ S.; 19° 50’ E.
Davis, G. M.; 17 Jan. 1978; salinity
Occ:

D78-74; large circular viei in the
Nuwejaarsrivier, about 1km. W of
Soetendalsvlei. Snails numerous on
marl bottom and on sedges; Cape
Prov.; 34° 43’ S.; 19° 58’ E. Davis, G.
M. and Dichmont, T.; 18 Jan. 1978;
Salinity ?

D78-73A; ме! next to the Nuwejaarsri-
vier at opening of river into Soeten-
dalsvlei; Agulhas region, Cape Prov.;
34° 44’ S.; 19° 58’ E. Davis, G. M.
and Dichmont, T.; 18 Jan. 1978;
salinity 0%.

D78-73B; in Nuwejaarsrivier oppo-
site vlei; salinity 07.0.

D78-65B; Langepan, where ме! exits
along road flowing to the east. On
road from Bredarsdorp to Elim,
16 km. from Bredarsdorp. Snails in
reeds; Cape Prov.; 34° 37’ 5.; 19°
54’ Е. Davis, G. M. and Dichmont, T.;
16 Jan. 1978; salinity 8°7/.0.

D78-4; De Hoopvlei on road from
Skipskop to Potbergsrivier. Snails on
sand, rocks, stems of grass and
algae; Cape Prov.; 34° 29’ S.; 20°
26’ E. Davis, G. M., Hoagland, K. E.
and Smits, J.; 2 Jan. 1978; salinity
5700.

APPENDIX 2. Systematics.

Tomichia ventricosa: type-species

Introduction—Anatomical data presented
for Т. ventricosa serve to define the genus as
well as the species. The only data discussed
for other species are those demonstrating dif-
ferences among species. The anatomy of
Tomichia ventricosa clearly indicates that this

genus

belongs to the Pomatiopsidae:

Pomatiopsinae as defined by Davis (1967,

244

DAVIS

TABLE 12. Shell measurements (mm) of species of Tomichia from specimens used for anatomical studies
yielding data in Tables 13-28. Mean + standard deviation; (range). N = 5 unless otherwise indicated.
eS

Length of Length of Width of
Species Length body whorl Width aperture aperture
T. differens
Females; 6.0-6.5 whorls 4.66 + 0.14 312 = 019 22748-084183 РИА ON? 1.38 + 0.12
(4.44 — 4.80) (2.92 - 3.28) (2.36 - 2.69) (2.0 - 2.28) (1.32 — 1.55)
М = 4 М = 4 NA!
Males; 6.0-6.5 whorls 4.92 + 0.36 3.06 + 0.16 2.48 + 0.12 281023012 1.34 = 0.06
(4.32 = 5:28) (2:8 - 3.2)" (24°=26 ) (1:92 — 2:28) (1:28 51.40)
T. natalensis
Females; 6.0-6.5 whorls 4.99 + 0.12 2.98 + 0.04 2.48 + 0.06 1.99 + 0.06 1.49 + 0.05
(4.88 — 5.12) (2.92 — 3.0 ) (2.40 - 2.50) (1.92 - 2.08) (1.4 — 1.52)
Males; 6 whorls 4.50 + 0.19 2.74 + 0.10 2.24 + 0.07 1.86 + 0.10 1.30 + 0.04
(4.4 —4.8 ) (2.68 - 2.88) (2.16 — 2.32) (1.72 — 2.0 ) (1.28 — 1.36)
T. rogersi
Females; 6.5-7.0 whorls 7.74 + 0.23 4.47 = 015 31542057 292=013 2108 = 0106
(7.44 — 7.92) (4.64 - 4.92) (3.28 — 3.76) (2.76 - 3.04) (2.04 — 2.16)
Ne 4 N= 4 NEA
Males; 7.0-7.5 whorls 8:6 = 0.26 5.02 + 0.09... 3.85 = 0.14 2.99 +0149, 222250107
(8.2 — 8.84) (4.88 - 5.12) (3.72 - 4.00) (2.83 — 3.20) (1.08 — 2.32)
T. tristis
Mixed males and fe- Teal se Oey СЦ == ОИ 2.52 + 0.14 1.76 + 0.07
males; eroded apices (6.08 — 8.08) (3.84 — 4.12) (3.2 - 3.48) (2.32 - 2.71) (1.72 — 1.88)
М = 7
Т. ventricosa
Females; 3 whorls 5.43 + 0.43 3.46 = 0.37 2.63 = 0.14 2.18 + 0.23 1.44 + 0.16
(eroded) (5.08 — 6.08) (2.88 — 3.76) (2.48 - 2.84) (2.00 — 2.52) (1.32 — 1.72)
Males 44 +0.38 2.90 + 0.29 2.09+0.21 1.76 + 0.18 1.16 = 0.10
(3.88 — 4.92) (2.52 — 3.32) (1.92 - 2.36) (1.52 — 2.00) (1.04 — 1.28)
М = 4
Т. zwellendamensis
Females; 7.5—8 whorls 5.41 + 0.32 PT) se 08 2.14 + 0.19 178220412 1.18 = 0.16
МЕ (5.0 — 5.68) (2.52 — 2.88) (1.88 — 2.32) (1.60 — 1.84) (0.96 — 1.36)
Males; 7.5-8 whorls 5.471020 260 012 2/08 1018 1.70 + 0.07 1.18 + 0.08
(5.20 — 5.72) (2.40 — 2.68) (1.96 — 2.24) (1.60 — 1.76) (1.08 — 1.36)

1968, 1979). Characters and character states
serving to define family and subfamily cate-
gories are not discussed here.

Shells (Figs. 7, 8)—Shells of mature adults
of the Ysterfontein population (Appendix 1,
V,) are invariably eroded, three to five whorls
but mostly three whorls. Statistics of shell
measurements are given in Table 12. The
length of the last three whorls is 5.46 +
0.34 mm (Fig. 12). Shape is turreted (Figs. 7,
8). Whorls moderately convex, sutures сог-
respondingly moderately impressed. Color
light brown to brown-yellow; shell glistening.
Aperture ovate (Fig. 13) lips moderately thick;
peristome complete with well-developed
parietal callus. Inner lip reflected from parietal

callus to abapical end of aperture; reflection
over umbilical and basal region of body whorl.
Reflection of lip at abapical end creates nearly
spout-like appearance. Due to reflection of in-
ner lip, broad arc of columella exposed inside
aperture.

Umbilicus varies from chink to widely open.
Shells mostly smooth (12x); some with pro-
nounced irregular growth lines. Spiral micro-
lines on some whorls of a few shells. Outer lip
with little or no sinuation (side view).

Shell of adults from Kleinrivier (Appendix 1,
Vg) differ from those discussed above as fol-
lows: all shells with eroded apices, two or
three whorls remaining. Color, dull brown due
to thick periostracum; thus shell not glistening.

POMATIOPSID EVOLUTION 245

TABLE 13. Length dimensions (mm) or number of non-neural organs of Tomichia ventricosa.

No. x Sd Range
Organ ($)
Body 5 8.70 0.64 7.6-9.2
Buccal mass 5 1.03 0.17 1.40-3.40
Anterior pallial oviduct 4 2.30 0.82 1.40-3.40
Posterior pallial oviduct 4 1.80 0.49 1.20-2.40
Total pallial oviduct (Po) 4 4.10 0.75 3.80-5.20
Bursa copulatrix (Bc) 5 1.18 0.15 1.00-1.40
Bc/Po 4 0.31 0.07 0.23-0.40
Seminal receptacle 5 0.16 0.03 0.14-0.20
Digestive gland 5 2.98 0.60 2.20-3.60
Gonad 4 1:23 0.33 0.90-1.60
Mantle cavity 4 2.87 0.43 2.60-3.50
Ctenidium 4 2.43 0.40 2.10-3.00
Gill filaments (no.) 5 55.4 1.67 54-58
Organ ($)

Body 5 7.02 1.31 5.8 -8.6
Prostate 5 1.07 0.20 0.76-1.30
Digestive gland 5 3.18 0.55 2.60-3.90
Gonad 5 3.06 0.50 2.60-3.90
Seminal vesicle 4 1.60 0.49 1.0 -2.20
Penis 5 1.63 0.39 1.20-2.10
Mantle cavity 5 2.34 0.24 2.00-2.60
Ctenidium 5 2.10 0.15 1.94-2.30
Gill filaments (no.) 5 39.8 2.28 36—42

Aperture an elongate oval (Fig. 13), lips thin,
outer lip very fragile. Parietal callus dips
slightly into and filling umbilicus of most
Shells. Inner lip slightly reflected; columellar
arc inside aperture not pronounced and nar-
rows to thin strip about mid-parietal callus.

Umbilicus lacking; <5% have chink. Shells
with regular discernable growth lines (12x).
Length of last three whorls 5.30 + 0.48 mm
(Fig. 12).

Organ measurements—See Table 13 for
measurements, counts, or ratios involving
non-neural organs or structures; Table 14 for
statistics on neural structures.

External features—The head (Fig. 14) is
densely pigmented except for the tip of the
snout (Sn). Scattered white glandular units
(С!) are concentrated around the eyes (Ey)
and extend a short distance out along the

LENGTH OF LAST THREE WHORLS

FIG. 12. Mean and standard deviation for length of
last three whorls (mm) plotted against the ratio
width: length of last three whorls. D, Tomichia dif-
ferens (topotypes); N, T. natalensis; В, T. rogersi 3
(topotypes); T, Т. tristis; V, T. ventricosa; Z, T. En =

zwellendamensis. WIDTH/ LENGTH OF LAST THREE WHORLS

246

FIG. 13. A demonstration of differences among taxa in aperture shape. А, В, Tomichia ventricosa (077-16);
C, D, T. ventricosa (D77-51); E, T. zwellendamensis (Note fold on columella); F, 7. tristis; G, T. rogersi
(topotypes); H, |, 7. natalensis; J, К, T. differens (topotype).

0.5 mm

FIG. 14. The head of Tomichia ventricosa. Ey, eye;
Gl, white glandular units; Ne, neck; Sn, snout; Tn, FIG. 15. Body whorls of 7. ventricosa demonstrat-
tentacle. ing dorsal strip of dense melanin pigment.

POMATIOPSID EVOLUTION 247
TABLE 14. Measurements (mm) of lengths of neural structures from female Tomichia ventricosa.
Structure No. x Sd Range
Cerebral ganglion 5 0.32 0.03 0.28-0.36
Cerebral commissure 5 0.25 0.03 0.20-0.28
Pleural ganglion—right (1) 5 0.18 0.03 0.16-0.22
—left 5 0.15 0.04 0.10-0.20
Pleuro-supraesophageal connective (2) 5 0.42 0.09 0.30-0.50
Supraesophageal ganglion (3) 5 0417 0.02 0.16-0.20
Osphradiomantle nerve 2 0.12 — 0.10-0.14
Pleuro-subesophageal connective 5 0.04 0.05 0.02-0.14
Subesophageal ganglion 5 0.14 0.02 0.12-0.16
Pedal ganglion 4 0.26 0.04 0.20-0.30
Pedal commissure 5 0.07 0.03 0.04-0.10
Statocyst (diameter) 5 0.11 0.01 0.10-0.12
Osphradial ganglion 4 0.48 0.07 0.40-0.56
Visceral ganglion 5 0.21 0.02 0.18-0.24
RPG ratio 5 0.54 0.04 0.48-0.59
tentacles (Tn). The dorsal aspect of the
whorls of the body have a dense pigment
band (Fig. 15).
Digestive system—Radular data are given
in Tables 15-17. SEM pictures of the radula
are given (Fig. 10). The radula is typically
pomatiopsid. The tip of the radular sac (Fig.
16, Trs) is directly beneath the central poste-
пог aspect of the buccal mass. Bed

Female reproductive system (Figs. 17-
20)—The uncoiled female is shown without
head and kidney tissue revealing the standard
pomatiopsine ground plan (Fig. 17). Cutting
across the mantle cavity and removing con-
nective tissues from the bursa copulatrix re-
veals organs as shown in Fig. 18. One clearly
sees the opening of the kidney (Oki) project-
ing into the rear of the mantle cavity. The
bursa copulatrix (Bu) is shown in the same
relationship to the pallial oviduct (Ppo) as in
Fig. 17. The bursa is extremely long, 31% the
length of the pallial oviduct (Table 13). The
anterior tip of the bursa (Tbu) extends into the
cavity of the kidney anterior to that point
where the oviduct passes into the posterior
pallial oviduct (= albumen gland) (Opo). The
tip of the bursa is within the narrowing funnel
of the kidney just before the kidney opens into
the mantle cavity.

The bursa copulatrix complex shown in
Figs. 19, 20 is in the same position as shown
in Figs. 17, 18. The interrelationships of the

—
FIG. 16. Dorsal buccal mass of A, T. ventricosa and
B, T. differens. Cg, cerebral ganglion; Dsg, duct of
salivary gland; Opt, optic nerve; Pig, pigmented re-
gion on dorsal buccal mass; Sg, salivary gland; SI,
supralabial nerve; Tn, tentacular nerve; Trs, tip of
radular sac.

Trs

DAVIS

248

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POMATIOPSID EVOLUTION 249

Ppo

Apo

FIG. 17. Female T. ventricosa, uncoiled, with head and kidney tissue removed. Apo, anterior pallial oviduct
(= capsule gland); Ast, anterior chamber of stomach; Bu, bursa copulatrix; Cl, columellar muscle; Di,
digestive gland; Edg, anterior end of digestive gland; Emc, posterior end of mantle cavity; Es, esophagus;
Go, gonad; In, intestine; Opo, opening to oviduct into posterior pallial oviduct (albumen gland); Ov, oviduct;
Ppo, posterior pallial oviduct (= albumen gland); Pst, posterior chamber of stomach; Sd, spermathecal duct;

Sts, style sac.

spermathecal duct (Sd), sperm duct (Зач),
seminal receptacle (Sr), oviduct (Ov), and
bursa are shown. In Fig. 19A, from a different
individual, the bursa was rotated slightly and
the oviduct at the opening to the pallial oviduct
(Opo) pulled through an arc of 90° toward the
observer from its position shown in Figs. 18,
19B to clearly show the position of the semi-
nal receptacle, the nature of the coils of the
sperm duct and oviduct. Note that the oviduct
is densely pigmented between the point
where the sperm duct connects and the open-
ing into the pallial oviduct (Fig. 19A, Pig).
My figure of the bursa complex (Davis
1979, fig. 9) is in error as it shows the sperm
duct (Sdu) connecting the oviduct to the

spermathecal duct as in Pomatiopsis, and as
it shows the seminal receptacle dorsal to the
bursa as in Pomatiopsis. This figure was from
dissections of two individuals in 1964 when |
was dissecting Pomatiopsis lapidaria. In fact
the sperm duct arises from the bursa copula-
trix close to, and anterior to the point where
the spermathecal duct enters the bursa. The
seminal receptacle tucks between the coils of
the sperm duct and the bursa on the ventral
surface of the bursa.

The opening (Op) of the pallial oviduct
(Apo) is shown together with the opening of
the spermathecal duct (Osp) (Fig. 19C).
These openings are at the anterior end of the
mantle cavity. The pallial oviduct produces a

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252 DAVIS

FIG. 18. Female T. ventricosa positioned exactly as in Fig. 17, but with the posterior stomach and digestive
gland removed posteriorly (to the left) and a cut across the body through the mantle cavity, pallial oviduct and
intestine (to the right) exposing the mantle cavity (Mc) and the structures within the cavity, e.g. opening of
kidney through posterior wall of the mantle cavity (Oki), cross sections of the esophagus (Es), posterior
pallial oviduct (Ppo), intestine (In), and spermathecal duct (Sd). The remaining gill filaments (Gf) of the
ctenidium are seen.

The purpose of the illustration is to show the relationship of the elongate bursa copulatrix (Bu) to the
posterior pallial oviduct (Pop), opening of the oviduct into the posterior pallial oviduct (Opo), and the anterior
tip of the bursa (Tbu) within the cavity of the kidney in the funnel of the kidney leading to the opening of the
kidney (Oki).

Au, auricle; Bu, bursa copulatrix; Emc, posterior end of the mantle cavity; Es, esophagus; Gf, gill filament;
Gn, gonadal nerve; In, intestine; Mc, mantle cavity; Oki, opening of kidney into the posterior mantle cavity;
Opo, opening of oviduct into posterior pallial oviduct; Ov, oviduct; Pe, pericardium; Ppo, posterior pallial
oviduct; Sbv, subvisceral connective; Sd, spermathecal duct; Sdu, sperm duct; Sts, style sac; Suv, supra-
visceral connective; Tbu, anterior tip of bursa copulatrix; Ve, ventricle; Vg, visceral ganglion; Wmc, reflected
cut wall of mantle cavity.

TABLE 17. General cusp formula for each species of South African Tomichia. ( )* = % of cusps.

Inner Outer
Taxon Central tooth Lateral tooth marginal marginal
T. differens 2(1) = 1—(1)2 3— 1 — 3(4) © = 18 9 — 11
2(3) — (3)2
Т. natalensis 2—1 =2 AE) = 1 = < 8—9 8—0
3.3
T. rogersi 22 2=1 =.3(4) 10 — 13 8—0
2(3) — (3)2
Т. tristis 21 —2 3 — 1 — (4)3 (66)* 11 = 12 910
DD 3— 1 —(2)8 (83)*
T. ventricosa AN 3(2) — 1 = 34) 10 — 15 8—1
2(3) — (3)2
Т. zwellendamensis = j= 2 3 == 3 12.— 14 i} = ik
2=2

RI _—o m nm m nn nn ЕЯ ЕЖЕ ДЖ SS

POMATIOPSID EVOLUTION 253

Sd
Sr

Apo

FIG. 19. Female reproductive system of Т. ventricosa. A, В, bursa copulatrix complex with bursa positioned
as in Figs. 17, 18. C, anterior end of pallial oviduct (Apo) showing the opening of the pallial oviduct (Op) at
the end of a nipple-like extension of the pallial oviduct. The opening (Osp) of the spermathecal duct (Sd) is
shown in relationship to the opening of the pallial oviduct.

In B, the positions of the ducts and organs are shown in usual configuration as in Fig. 18. In A, the oviduct
at the pallial oviduct (Opo) has been shown pulled 90° towards the reader to show the seminal receptacle
(Sr) in its usual position. Note the densely pigmented (Pig) section of the oviduct where it opens into the
pallial oviduct.

Apo, anterior pallial oviduct; Op, anterior opening of pallial oviduct; Opo, opening of oviduct into the
posterior pallial oviduct; Osp, anterior opening of spermathecal duct; Ov, oviduct; Pig, pigmented section of
oviduct; Sd, spermathecal duct; Sdu, sperm duct; Sr, seminal receptacle.

254 DAVIS

0.6mm

FIG. 20. Bursa copulatrix complex as in Fig. 19. A-C, T. natalensis; D, Е, T. rogersi. The spermathecal duct
enters the posterior bursa in T. natalensis. The posterior bursa is particularly elongate in T. rogersi. В, the

coils of the oviduct and path of sperm are shown.

Bu, bursa copulatrix; Dsr, duct of seminal receptacle; Opo, opening of oviduct into posterior pallial oviduct;
Ov, oviduct; Sd, spermathecal duct; Sdu, sperm duct; Sr, seminal receptacle.

nozzle-like extension at the anterior end of the
pallial oviduct at the tip of which is the open-
ing.

Male reproductive system (Figs. 21, 22)—
The system is standard pomatiopsine. Penis
with eversible papilla, ciliated anterior epitheli-
um and glandular edge on proximal concave
curvature (Fig. 22) The vas deferens does not
have a thickened ejaculatory section either in
the base of the penis or proximal to the base
of the penis.

Nervous system—The nervous system is
standard pomatiopsid. Measurements of
neural structures are given in Table 14. The
RPG ratio (Table 14) is 0.54, significantly
larger than that in Oncomelania and
Pomatiopsis and similar to that recorded for
Hydrobia (Davis et al., 1976). This larger ratio
is due to a comparatively long pleuro-supra-
esophageal connective and indicates a more
Open (as opposed to condensed) central
nervous system.

POMATIOPSID EVOLUTION 255

Pst

FIG. 21. Male reproductive system of T. ventricosa. Head and kidney tissue were removed. Part of the gonad
(Go) was removed to reveal the coiled seminal vesicle (Sv).

Ast, anterior chamber of stomach; Cl, columellar muscle; Di, digestive gland; Emc, posterior end of the
mantle cavity; Es, esophagus; Go, gonad; In, intestine; Ma, mantle edge = collar; Pc, pellet compressor; Pr,
prostate; Pst, posterior chamber of stomach; Sts, style sac; Sv, seminal vesicle; Vd,, vas deferens posterior
to prostate; Vdo, vas deferens anterior to prostate; Ve, vas efferens.

FIG. 22. Penis of T. ventricosa. Ci, cilia; Сие, glandular edge of the penis; Gl, subepithelial gland types; Pa,
papilla; Vd, vas deferens.

256 DAVIS

T. differens

Shell (Fig. 8)—Type-locality (Appendix 1,
D,) not much eroded, males and females 6.0
to 6.5 whorls. Statistics in Table 12. Length of
last three whorls 4.25 + 0.14 mm (Fig. 12).
Shape ovate (bullet-shaped). Whorls Нан
sided to slightly convex, sutures shallow.
Color light brown, glistening. Aperture ovate-
pyriform with produced adapical end (Fig. 13),
lips thick, peristome complete with thick
parietal callus. Inner lip not reflected; abapical
end of aperture projecting slightly below base
of body whorl. Slight arc of columella seen
inside aperture.

No umbilicus or only a chink(<5%). Smooth
body and penultimate whorl (about 40%).
Outer lip straight or with slight sinuation (side
view).

Organ measurements—See Table 18 for
measurements or ratios of non-neural organs;
Table 19 for measurements of neural struc-
tures.

Unique features—The tip of the radular sac
extends beyond the end of the buccal mass
and curls dorsally between the cerebral nerv-
ous system and the buccal mass (Fig. 16B,
Trs). Other aspects as in 7. ventricosa.

Radula—See Fig. 9, Tables 15-17.

T. natalensis

Shell (Fig. 7)—Locality (N3, Appendix 1),
invariably entire with males 6.0 whorls and
females 6.0 to 6.5 whorls. Statistics, Table 12.
Length of last three whorls 4.10 + 0.22 (Fig.
12). Shape ovate-conic. Whorls moderately
convex, sutures correspondingly impressed.
Color dark brown due to heavy periostracum.
Peristome entire, with dark brown edge, thick.
Aperture shape variable, widely ovate to sub-
quadrate, slightly produced at adapical end in
some specimens. Parietal callus well formed,
straight to slightly sinuate. Inner lip not re-
flected over umbilical or basal areas of the
body whorl. Inside aperture only very narrow
strip of columella seen (Fig. 13).

No umbilicus; a few with chink. Shells
smooth, dull, without pronounced growth
lines, no spiral micro-lines. Outer lip of most
shells with marked sinuation.

Organ measurements—See Table 20 for
non-neural organs; Table 21 for neural struc-
tures.

Radula—See Fig. 9, Tables 15-17.

Unique features—The spermathecal duct
enters the bursa at, or close to the posterior
end of the latter (1) (Figs. 20A, C) and is sepa-
rated from the opening of the sperm duct into

TABLE 18. Dimensions (mm) or number of non-neural organs of topotype Tomichia differens, D 77-13.

No.

Organ ($)
Body
Buccal mass
Anterior pallial oviduct
Posterior pallial oviduct
Total pallial oviduct (Po)
Bursa copulatrix (Bc)
Bc/Po
Seminal receptacle
Digestive gland
Gonad
Mantle cavity
Ctenidium
Gill filaments

Organ (3)
Body
Prostate
Digestive gland
Gonad
Seminal vesicle
Penis
Mantle cavity
Ctenidium
Gill filaments

a oe a eee oe Pi u
O1 B O1 B O1 & O O UN

A ТГ ST ls
O1 O1 O1 O1 B O BP 01 Ur

x Sd Range
8.32 0.36 8.0 -8.8
1.01 0.16 0.9 -1.3
1255 0.12 1.4 —1.7
1.95 0.10 1.8 -2.1
3.50 0.17 3.3 -3.8
1.11 0.11 1.0 -1.28
0.31 0.04 0.26-0.37
0.14 0.03 0.10-0.16
3:32 0.22 3.0 -3.6
1.05 0.28 0.9 —1.1
2,92 0.13 2.1 -2.4
1.82 0.27 1.6 -2.2

28.8 2.86 25-32
8.92 0.76 8.0 -9.6
0.88 0.25 0.5 -1.20
4.88 0.83 4.0 -6.0
4.72 0.62 4.0 -5.4
1.40 0.28 1.0 -1.6
1.94 0.38 1.5 -2.5
2.22 0.15 2.0 -2.4
1.72 0.08 1.6 -1.8

27.6 2.60 26-32

POMATIOPSID EVOLUTION

the bursa by 0.26mm or more, usually
0.30 mm. (2) In T. ventricosa this distance is
usually 0.20 mm or less. (3) The opening of
the sperm duct into the bursa is at the left
ventro-lateral edge of the bursa or on the left
dorso-lateral edge instead of mid-ventral
bursa (Figs. 20A, C).

T. rogersi

257

Shell (Fig. 7)—Type-locality (Appendix 1,
R,). Mostly entire, males 7.0-7.5 whorls, fe-
males 6.5-7.0 whorls. Statistics in Table 12.
Length of last three whorls 6.84 + 0.18 тт
(Fig. 12). Shape turreted. Whorls moderately

TABLE 19. Measurements (mm) of lengths of neural structures from female Tomichia differens.

Structure No. X Sd Range
Cerebral ganglion 5 0.35 0.04 0.30-0.40
Cerebral commissure 5 0.22 0.06 0.16-0.30
Pleural ganglion—right (1) 5 0.16 0.01 0.14-0.16
—left 5 0.15 0.01 0.14-0.16
Pleuro-supraesophageal connective (2) 5 0.30 0.07 0.20-0.38
Supraesophageal ganglion (3) 5 0.15 0.02 0.14-0.18
Osphradiomantle nerve 5 0.16 0.06 0.10-0.20
Pleuro-subesophageal connective 5 0.03 0.03 0 -0.06
Subesophageal ganglion 5 0.14 0.03 0.10-0.16
Pedal ganglion 5 0.26 0.11 0.20-0.32
Pedal commissure 5 0.08 0.02 0.04-0.10
Statocyst (diameter) 3 0.11 0.01 0.10-0.12
Osphradial ganglion TA 0.42 0.06 0.32-0.48
Visceral ganglion 4 0.15 0.01 0.14—0.16
RPG ratio: 2/1 + 2 + 3 5 0.49 0.06 0.40-0.56
TABLE 20. Length dimensions (mm) or number of non-neural organs of Tomichia natalensis.
No. x Sd Range
Organ ($)
Body 4 8.2 0.58 7.6 -8.7
Buccal mass 5 0.92 0.02 0.9 -0.94
Anterior pallial oviduct 3 1.53 0.15 1.4 -1.7
Posterior pallial oviduct 3 1.75 0.05 1.7 -1.8
Total pallial oviduct (Po) 4 3.18 0.10 3-33
Bursa copulatrix (Вс) 5 1.26 0.06 1.2. =1.3
Вс/Ро 4 0.40 0.02 0.38—0.42
Seminal receptacle 1 0.20 — —
Digestive gland 4 3.45 0.24 3.2 -3.7
Gonad 3 1.20 0.17 1.0 -1.3
Mantle cavity 4 2.63 0.29 2.3 -3.0
Ctenidium 4 2.03 0.29 1.7 -2.4
Gill filaments 4 37.8 2.29 35—40
Organ ($)
Воду 2 8.0 — 7.8 3.2
Prostate 2 1.35 — 1.3 -1.4
Digestive gland 2 3.7 — 3.6 -3.8
Gonad 2 3.0 — 0
Seminal vesicle 2 1.1 — 0
Penis 3 2:77 0.55 2.4 -3.4
Mantle cavity 2 2.85 — 2.7 —3.0
Ctenidium 2 2.40 — 0
Gill filaments 2 30 — 0

258 DAVIS

convex, sutures correspondingly impressed.
Color yellow brown, without heavy periostra-
cum and surface thus glistening. Peristome
complete, lips thickened but without dark
brown edge. Aperture ovate, not produced at
adapical end (Fig. 13); inner lip not reflected
over umbilical or basal areas of the body
whorl. Parietal callus well formed, straight or
arcuate. Inside aperture columella not seen or
only very narrow strip seen.

Umbilicus lacking, a chink, or moderately
open. Shells smooth, without pronounced

growth lines. Some shells have spiral micro-
lines while others (<5%) have oddly spaced
raised micro-cords that give area of the shell a
malleated appearance. Outer lip of most
shells straight or with very slight sinuation
(side view).

Organ measurements—See Table 22 for
non-neural organs; Table 23 for neural struc-
tures.

Radula—See Fig. 9, Tables 15-17.

Unique features—1) large size, 2) the bursa
posterior to the opening of the spermathecal

TABLE 21. Measurements (mm) of lengths of neural structures from male Tomichia natalensis. N = 4.

Structure X Sd Range
Cerebral ganglion 0.22 0.02 0.30-0.24
Cerebral commissure 0.09 0.01 0.08-0.10
Pleural ganglion—right (1) 0.12 0.03 0.10-0.16

—left 0.22 0.08 0.16-0.34
Pleuro-supraesophageal connective (2) 0.36 0.03 0.34-0.40
Supraesophageal ganglion (3) 0.15 0.03 0.12-0.18
Osphradiomantle nerve 0.11 0.03 0.08-0.16
Pleuro-subesophageal connective 0.14 0.07 0.08-0.20
Pedal ganglion 0.21 0.01 0.02-0.22
Pedal commissure 0.09 0.01 0.08-0.10
Statocyst (diameter) 0.10 0.01 0.08-0.10
Osphradial ganglion (N = 3) 0.58 0.06 0.52-0.64
RPG ratio 0.57 0.04 0.52-0.61

TABLE 22. Length dimensions (mm) or number of non-neural organs of topotype Tomichia rogersi.

No.

Buccal mass

Anterior pallial oviduct
Posterior pallial oviduct
Total pallial oviduct (Po)
Bursa copulatrix (Bc)
Bc/Po

Seminal receptacle
Digestive gland

Gonad

Mantle cavity
Ctenidium

Gill filaments

Organ ($)
Body
Prostate
Digestive gland
Gonad
Seminal vesicle
Penis
Mantle cavity
Ctenidium
Gill filaments

O1 O1 O1 O1 O1 O1 On On On 6 1 O1 O1 O1

O1 O1 O1 O1 O1 O1 O1 O1 On

X Sd Range
12.28 1.07 10.6 -13.4
1.30 0.14 1.1 — 1.40
2.56 0.71 2.0 - 3.80
2.26 0.09 2:2 =12"4
4.82 0.79 4.2 - 6.2
1.70 0.11 1.6 - 1.8
0.36 0.04 0.29- 0.40
0.27 0.03 0.24- 0.30
5.02 0.23 4.8 - 5.3
2.26 0.33 2.0 - 2.8
4.16 0.09 4.0 - 42
3.70 0.14 3.5 - 3.8
51.6 2.70 50-55
12.58 0.78 11.9 -13.8
1.28 0.11 1.20- 1.40
6.84 0.32 6.34- 7.0
7.24 0.43 7.0 - 8.0
3.04 0.52 2.4 - 3.8
2.36 0.40 1.8 - 29
4.04 0.26 3.8 - 4.4
3.46 0.26 3.2 — 3.8
50.6 4.44 45-56

POMATIOPSID EVOLUTION 259

TABLE 23. Measurements (mm) of lengths of neural structures from female Tomichia rogersi.

Structure No. X Sd Range
Cerebral ganglion 5 0.36 0.03 0.32-0.40
Cerebral commissure 5 0.27 0.03 0.24-0.30
Pleural ganglion—right (1) 5 0.18 0.02 0.16-0.20

—left 5 0.21 0.02 0.20-0.24
Pleuro-supraesophageal connective (2) 5 0.62 0.15 0.50-0.88
Supraesophageal ganglion (3) 5 0.20 0.02 0.18-0.22
Osphradiomantle nerve 3 0.18 0.03 0.14—0.20
Pleuro-subesophageal connective 5 0.08 0.11 0.02-0.28
Subesophageal ganglion 5 0.18 0.03 0.12-0.20
Pedal ganglion 5 0.30 0.03 0.26-0.34
Pedal commissure 5 0.08 0.04 0.02-0.10
Statocyst (diameter) 5 0.14 0.02 0.12-0.16 -
Osphradial ganglion 5 0.71 0.08 0.60-0.80
Visceral ganglion 4 0.25 0.02 0.22-0.26
RPG ratio: 2/1 + 2 +3 5 0.61 0.06 0.57-0.71

TABLE 24. Measurements of individual shells of Tomichia tristis with entire whorls.

Length of
Length of Length of Width of last three
Whorl no. Length Width body whorl aperture aperture whorls
7:5 6.52 3.0 3.6 232 1.64 5.4
1745 6.00 2.6 3.16 1.92 1.48 4.72
TES 6.80 22908 3.84 2.40 1572 5.52
TES 7.08 3.04 3.88 2.52 1.68 5.68
8.0 7.28 3.08 3.8 2.44 1872 5.68
TABLE 25. Length dimensions (mm) or number of non-neural organs of Tomichia tristis.
No. x Sd Range
Organ ($)
Body 4 12.63 1.82 11.3 -15.2
Buccal mass 3 18 0.10 1.2 - 1.4
Anterior pallial oviduct 4 2.0 0.33 1.6 - 2.4
Posterior pallial oviduct 4 2.53 0.49 1.8 - 2.8
Total pallial oviduct (Po) 4 4.53 0.28 4.2 - 4.8
Bursa сорщашх (Вс) 4 1.42 0.06 1.36- 1.50
Вс/Ро 4 0.32 0.02 0.29- 0.35
Seminal receptacle 3 0.29 0.12 0.20- 0.42
Digestive gland 4 4.75 0.81 3.6 - 5.4
Gonad 3 1.97 0.21 1.8 - 2.2
Mantle cavity 4 3.95 0.41 3.4 - 4.4
Ctenidium 4 3.61 0.29 3.4 - 4.4
Gill filaments (no.) 4 56 2.94 52-59
Organ ($)
Body 2 114 — 10.6 -11.6
Prostate 1 172 — —
Digestive gland 2 57. = 4.6 - 6.8
Сопаа 1 4.8 — —
Seminal vesicle — — — =
Penis 2 2.35 — 1.6 - 3.1
Mantle cavity 2 3.4 — 3.0 - 3.8
Ctenidium 2 3.0 — 2.6 - 3.4
Gill filaments (no.) 2 57.5 — 56-59

260 DAVIS

duct is frequently elongate, >0.70 mm (Figs.
20D, E); it is about 0.40 mm (and rarely at-
tains 0.60) in Т. ventricosa.

T. tristis

Shells (Fig. 7)— Various degrees of erosion
of apical whorls. Mixed mature males and fe-
males with eroded apices measured 8.15 +
0.67 тт length. Statistics, Tables 12, 24.
Length of last three whorls 5.68 + 0.29 тт
(Fig. 12). Shape turreted. Whorls slightly con-

vex to straight-sided. Sutures moderately
shouldered. Color brown or dull yellow brown;
periostracum moderate but sufficient to make
shells dull. Peristome complete, lips moder-
ately thickened, without dark brown edge.
Aperture narrowly ovate, not produced adapi-
Cally (Fig. 13). Inner lip slightly reflected over
umbilical and basal areas of the body whorl.
Parietal callus well formed, arcuate or
straight, but sunk below the curvature of the
body whorl. Inside aperture columellar strip
prominent because of inner lip reflection.

TABLE 26. Measurements (mm) of lengths of neural structures from male and female Tomichia tristis. N = 4.

Structure

Cerebral ganglion
Cerebral commissure
Pleural ganglion—right (1)

—left
Pleuro-supraesophageal connective (2)
Supraesophageal ganglion (3)
Osphradiomantle nerve
Pleuro-subesophageal connective
Pedal ganglion (N = 2)
Statocyst (diameter) (N = 1)
Osphradial ganglion (N = 3)
Visceral ganglion
RPG ratio 2/1 +2 +3

x Sd Range
0.35 0.02 0.32-0.36
0.26 0.04 0.20-0.30
0.19 0.02 0.16-0.20
0.18 0.03 0.14-0.20
0.50 0.09 0.40-0.60
0.18 0.03 0.14-0.20
0.13 0.03 0.10-0.16
0.13 0.15 0.02-0.34
0.29 — 0.28—0.30
0.10 —- ==
0.77 0.18 0.60-0.96
0.61 0.09 0.50-0.72

TABLE 27. Length dimensions(mm) or number of non-neural organs of Tomichia zwellendamensis.

No.

Organ (<)
Body
Prostate
Digestive gland
Gonad
Seminal vesicle
Penis
Mantle cavity
Ctenidium
No. filaments

— — = N N = = WO —

X Sd Range
8.4 0.75 7.6 - 9.6
0.88 0.19 0.74- 1.1
2.16 0.42 1.7 - 2.8
1.63 0.34 1.4 - 22
3.83 0.42 3.36- 4.20
1.09 +0.23 0.80- 1.4
0.29 0.04 0.23- 0.33
0.19 0.02 0.16- 0.20
3.07 0.30 2.6 — 3.4
1.3 0.10 1.2 - 1.4
2.85 0.40 2.2 - 3.2
2.57 0.41 1.96- 2.80
51.2 8.1 40-62
9.0 == tay
1.07 — 1.01- 1.14
4.8 — —

4.8 — —

1.0 — —

1.5 = 1.3 - 1.7
2.8 — —

gia — —
66 — —

POMATIOPSID EVOLUTION 261

TABLE 28. Measurements (mm) of lengths of neural structures from male and female Tomichia zwellenda-

mensis. N = 3.
Structure

Cerebral ganglion
Cerebral commissure
Pleural ganglion—right (1)

—left
Pleural-supraesophageal connective (2)
Supraesophageal ganglion (3)
Pleural-subesophageal connective
Subesophageal ganglion (N = 2)
Pedal ganglion
Pedal commissure
Statocyst (diameter)

Osphradial ganglion (N = 5)
Visceral ganglion
RPG ratio: 2/1 + 2 + 3

Shells with umbilical chink to wide open
umbilicus. Shell surface rough, some shells
with pronounced growth lines, many (60%)
with malleation on the body whorl. Spiral
micro-striations common. Outer lip sinuate
(side view).

Organ measurements—See Table 25 for
non-neural organs; Table 26 for neural struc-
tures.

Radula—See Fig. 10, Tables 15-17.

Unique features —none.

T. zwellendamensis

Shells (Fig. 8)—Locality (Appendix 1, Zs),
varying degress of erosion of apical whorls.
Mature males and females 7.5 to 8.0 whorls.
Statistics on shell measurements, Table 12.
Length of last three whorls 4.06 + 0.19 mm
(Fig. 12). Shape, slender-turreted. Whorls
moderately to quite convex; sutures deep.
Color straw yellow. Periostracum slight, shells
very fragile and translucent. Peristome not
complete in >90%; if complete, only a hint of
a parietal callus. Lips thin, without dark brown
edge. Aperture ovate, not produced adapical-
ly (Fig. 13). Inner lip slightly reflected over
umbilical and basal areas of the body whorl;
slight arc of columella seen inside aperture
because of this slight reflection.

Shells not umbilicate. Shell surface smooth,
rarely with growth lines. Twist in columella
evident in many shells where outer lip starts
reflection. Outer lip straight (side view).

Organ measurements—See Table 27 for
non-neural organs; Table 28 for neural struc-
tures.

x Sd Range
0.26 0.02 0.24—0.28
0.13 0.04 0.10-0.18
0.1 0 0
0.11 0.02 0.09-1.2
0.23 0.07 0.16-0.30
0.11 0.01 0.08-0.10
0.02 0.02 0 -0.02
0.11 — 0.09-1.2
0.20 0.02 0.18—0.22
0.03 0.03 0 -0.06
0.09 0.01 0.08—0.10
0.47 0.09 0.34-0.56
0.51 0.07 0.44—0.58

Radula—See Fig. 10, Tables 15-17.
Unique features—only some shell char-
acter-states.

APPENDIX 3. Types examined and the status
of Tomichia cawstoni

Types examined:

Hydrobia alabastrina Morelet, 1889: 19, pl. 2,
fig. 5. British Museum (Nat. Hist.); ex-
amined 9 February 1978. Mixed lot; small
specimen is Rissoa capensis Sowerby,
1892. Holotype as figured by Connolly,
1939.

Tomichia cawstoni Connolly, 1939: 585, text
fig. 48L, British Museum (Nat. Hist.); ex-
amined 9 February 1978. The shell is yel-
low, straight and flat-sided, not umbilicate,
very Tricula-like.

Tomichia differens Connolly, 1939: 583, text
fig. 47M, South African Museum; examined
circa 14 November 1977. Material indistin-
guishable from my collections at the type
locality, D77-13, 19 November 1977.

Assiminea аа Turton, 1932: pl. 35, fig.
1097. Zoological Museum, Oxford Univer-
sity; examined 10 February 1978. Holotype
figured. This shell phenotype is the same
seen in some individuals of a single popu-
lation where other shells clearly resemble
Tomichia tristis, described and figured by
Morelet, 1889: 18, pl. 2, fig. 4, and Con-
nolly, 1939.

262 DAVIS

Tomichia natalensis Connolly, 1939: 586, text
fig. 470. British Museum (Nat. Hist.), ex-
amined 9 February 1978.

Tomichia producta Connolly, 1929: 242, pl.
14, fig. 40. British Museum (Nat. Hist.); ex-
amined 9 February 1978. Specimen clearly
referable to Т. ventricosa.

Hyrobia rogersi Connolly, 1929: 242, pl. 14,
fig. 41. South African Museum; examined
circa 14 November 1977.

Tomichia cawstoni was described from
Kokstad, Cape Province. Kokstad is a small
highland community situated N of national
road Ro, to the east of the Transkei, close to

the border of Natal Province. Dr. David Brown
(now of the British Museum (Natural History))
and | have both searched for this species and
have not located it. | examined stream banks,
streams, and marshes around the area of
Kokstad to no avail. There are very few
streams in this region and Kokstad is situated
in an isolated pocket in the hills.

A stream-marsh area along the main high-
way (Ro) opposite the turnoff to Kokstad ap-
peared to provide a suitable habitat. This
area, upon inspection, was polluted with oil.
The fields surrounding were extensively used
for grazing cattle. | presume this species to be
extinct.

MALACOLOGIA, 1981, 21(1-2): 263-289

ANATOMY, BIOLOGY AND SYSTEMATICS OF CAMPANILE SYMBOLICUM
WITH REFERENCE TO ADAPTIVE RADIATION OF THE
CERITHIACEA (GASTROPODA: PROSOBRANCHIA)

Richard S. Houbrick

Department of Invertebrate Zoology, National Museum of Natural History,
Smithsonian Institution, Washington, D.C. 20560, U.S.A.

ABSTRACT

Campanile symbolicum Iredale is the sole survivor of a long lineage of large mesogastropods
in the family Campanilidae. The family was well represented in the Tethys Sea and underwent a
widespread adaptive radiation in the early Tertiary. Several of the fossil species are among the
largest known gastropods. The living relict is confined to southwestern Australia where it is
common in shallow, subtidal, sandy habitats. It is a herbivore with a generalized taenioglossate
radula and thick jaws. The large, elongate conical shell has a chalky periostracum and the
aperture, which has a central anterior canal, is at a 45 degree angle to the shell axis. The open
pallial gonoducts in both sexes and aphallic males are conservative characters found in all
cerithiaceans. These, and the characters derived from the shell, operculum and radula un-
equivocally refer Campanile to the superfamily Cerithiacea. Anatomical features of the sensory,
reproductive, alimentary and nervous systems of Campanile are unique among the Cerithiacea
and indicate that it should be allocated to a separate family, the Campanilidae.

Among the external anatomical features peculiar to Campanile are a short thick snout, tiny
eyes, and a deep ciliated pedal gland around the entire margin of the sole of the foot. Small
papillae surround the entire mantle edge. The columellar muscle is long and has a large promi-
nence. A short oval bipectinate osphradium is located at the anterior end of the mantle cavity

‘ adjacent to the long ctenidium. It closely resembles the osphradia of neogastropods and several
families of higher mesogastropods. The hypobranchial gland is modified into tiny leaflets where it
is adjacent to the anus. Two simple laminae comprise the pallial oviduct and are longitudinally
folded. The internal folds of the proximal end of the left lamina of the pallial oviduct are elaborat-
ed into broadly ovate transverse ridges forming a large albumen gland. A sac-like seminal
receptacle projected into the pericardial sac opens into the left proximal end of the pallial oviduct.
It occurs in both sexes but is more highly developed in females. Although sexes are separate,
this suggests that Campanile is a protandric hermaphrodite. The head and foot of a mature
animal become bright pink. It appears that Campanile forms spermatophores. Sperm taken from
the vas efferens are all eupyrene. Spawn masses are large gelatinous tubes deposited on the
substratum and contain spirally arranged capsules, each of which contains one to several
moderately sized eggs. Development is either direct or with a short demersal larval stage.
Veliger stages are attained within the spawn mass and the embryonic shell is smooth, bulbous
and lacks a sinusigera notch. The radula of Campanile is wide and robust but unusually short in
comparison to the size of the snail. Paired salivary glands and their ducts and paired buccal
pouches lie anterior to the nerve ring. The mid-esophagus encloses the dorsal and ventral food
channels. It has shallow lateral folds but no esophageal gland and is surrounded by a large mass
of connective tissue in the middle of which is a thin muscular sheet. The stomach has a style sac
but lacks a gastric shield and a style. In the sorting area is a series of leaflets spirally arranged
in a deep pit. In the posterior of the stomach is the vestige of a spiral caecum. The nervous
system comprises a mixture of loosely connected and condensed ganglia and is dialyneurous
and zygoneurous.

The Campanilidae appeared in the late Cretaceous to early Tertiary as did most other sub-
stantial cerithiacean families. Each family radiated into a specific adaptive niche and has re-
mained essentially the same in ecology and general physiognomy of its members. Although the
Campanilidae were abundant in the Paleocene and Eocene, it is the only cerithiacean family to
have undergone serious diminution in species to the point of virtual extinction. Campanilid snails
were the largest animals in the superfamily and were undoubtedly grazers of microalgae in the
shallow waters of the Tethys. A hypothesis for the demise of the Campanilidae is trophic
competition with another group of large grazing gastropods, the Strombidae, which became
established in the late Eocene to early Miocene and flourished in a similar ecological niche.

(263)

264
INTRODUCTION

During the early Tertiary, genera of the fam-
ily Campanilidae Douvillé, 1904, were a group
of many species that were common in the
Tethys Sea. There is an extensive literature
about these spectacular gastropod fossils.
Some species, such as Campanile gigante-
um (Lamarck, 1804), attained a length of 1 m
and are among the largest gastropods on
record. The family is represented today by a
single living species: Campanile symbolicum
Iredale, 1917, from southwestern Australia.

This living species is a subtidal, shallow-
water dweller that is common within its limited
range. Although it is unusually large for a
cerithiid, and a relict species of an extinct
group, it is not well known to malacologists
and is poorly represented in museum collec-
tions outside Australia. Virtually nothing has
been published about its ecology or life his-
tory and no recent comprehensive account of
the anatomy of this interesting animal exists;
consequently, its relationship to other cer-
ithiacean groups and to the numerous fossil
species within the family Campanilidae is con-
jectural and is based solely on shell charac-
ters. Indeed, some authors have questioned
whether Campanile symbolicum is of the
same lineage as the larger Tethyan fossils.

Much of the literature on this group has
dealt with the selection of a proper type-
species for the genus and with nomenclatural
problems. The nomenclature of the generic
and specific names has a complex history.

In May, 1979, | observed a population of
Campanile symbolicum at Pt. Peron, near
Perth, Western Australia. | studied the living
animals and dissected narcotized specimens
in order to make anatomical comparisons with
other cerithiaceans. Egg masses and em-
bryos were also studied.

This paper presents my findings and in-
cludes an historical review of the genus
Campanile. My description of Campanile
symbolicum includes anatomical, embryo-
logical, opercular and radular characters as
well as shell features. | also include some
aspects of the reproductive biology and brief
notes on the ecology of the species. These
findings indicate that Campanile should be
assigned to a separate family, Campanilidae.
The relationship of this relict family to other
families within the Cerithiacea reflects the
adaptive radiation of the superfamily.

HOUBRICK

MATERIALS AND METHODS

Specimens were collected by hand while
snorkeling from Pt. Peron, Western Australia
and living animals were examined in the field
to determine their exact habitat. Individual
snails were maintained in seawater aquaria at
the Western Australian Museum, Perth, for
behavioral observations. For anatomical
studies, animals were extracted from their
shells that had been cracked with a large vise
and were relaxed in 7.5% MgCl». Dissections
were made with the aid of a binocular dissect-
ing microscope. Material for histological sec-
tions was prepared in Bouin's Fixative, em-
bedded in paraffin and sectioned on the mi-
crotome at 5 um. Sections were stained with
Harris’ hematoxylin and counterstained with
Eosin Y. The radula, jaws, periostracum and
shell ultrastructure were studied with a scan-
ning electron microscope. The geographic
range of the species was determined by ex-
amination of specimens in major museums in
the United States and Australia, and statistics
of shell measurements computed from a large
series of adult shells. Preserved spawn
masses and embryos were studied with a
Wild stereo dissection scope and a scanning
electron microscope was used to study em-
bryonic shells.

KEY TO ABBREVIATIONS ON FIGURES

a --anus

aa — ащепог aorta

ag — абитеп gland

as —attachment surface

au —auricle

b —baffle

bg —buccal ganglion

bm —buccal mass

bp —buccal pouch

Бу —blood vessel

cem —cut edge of mantle

cf —ciliated furrow

cm —columellar muscle

cnt —connective tissue

ct —ctenidium

ctb —ciliated tube

ctr —<ciliated tract

dg —digestive gland

dol —division of outer lamina
dpg —distal part of pallial oviduct
—duct of seminal receptacle

CAMPANILE ANATOMY AND SYSTEMATICS 265

ebv —efferent branchial vessel
es —esophagus

eso —esophagus opening

ev —esophageal valve

exs —exhalant siphon

f —foot
ff —fold emerging from spiral caecum
fg —food groove

FL —sperm flagellae
gil —glandular part of inner lamina
gs —-"gastric shield”
gsa —grooved channel
—head of sperm
hg —hypobranchial gland
| —inner lamina
ins —inhalant siphon
int —-opening to intestine
iF jaw
к —kidney
ko —kidney opening
Icg —left cerebral ganglion
Id —lower duct
les —lumen of esophagus
Ing —leaflets of hypobranchial gland
lpg —left pleural ganglion
рп —left pallial nerve
mc —mantle cavity
me —mid-esophagus
ml —thin muscular layer
mp —mantle papillae
od —odontophore
odg —oviducal groove
odu —oviduct
OES—opening to esophagus
ol —outer lamina
op —operculum
opn —optic nerve
os —osphradium
osr —opening of seminal receptacle
OV —ovary
pp —propodium
ppg —proximal part of pallial oviduct
ps —pericardial sac

г —rectum

ra —radula

rcg —right cerebral ganglion

rl ©—renal lamellae as seen by transparency

rpd —renopericardial duct

rpg —right pleural ganglion

RW —receptacle wall

sa —sorting area

sc —spiral caecum

sec —supraesophageal connective
seg —supraesophageal ganglion
sg —salivary gland

sl —sorting leaflets

sn —snout

sp —sperm in smooth chamber
sr —seminal receptacle

ss —style sac

st —stomach

t; —major typhlosole

{> —minor typhlosole

tn —tentacle nerve

ve —ventricle

wps —wall of pericardial sac

Z —zygoneury between right pleural gan-
glion and subesophageal ganglion.

DESCRIPTION

This section deals with the descriptions of
the shell, operculum, radula, anatomy, spawn
and larvae of Campanile symbolicum, and
will bring together my own observations and
those of previous authors. The anatomical
description includes external and internal fea-
tures and is supplemented with histological
studies. The functional interpretations of vari-
ous systems are proposed and most of the
significant anatomical features are figured.
Brief discussions on ecology and the fossil
history of Campanile are included.

Specimens examined-Great Australian
Bight (ММУ); Recherche Archipelago,
23°15'S, 122°50’E, including Mondrain ld.,
Salisbury Id., Middle Id., Boxer Id. (all NMV);
Nares Id., Duke of Orleans Bay (WAM); Lucky
Bay (WAM); Two Mile, Hopetoun (AMS,
WAM); Bremer Bay (WAM); Princess Royal
Harbour (AMS); Pallinup River Estuary
(WAM); Point Irwin (DMNH); South Point, $
side of Two People Bay, Albany (AMS); Irwin
River Inlet, W of Albany (AMS); Middletown
Beach, Albany (WAM); Frenchman's Bay,
Albany (WAM); Albany (ANMH); Cowaramup
Bay (AMNH); Augusta (WAM); Sarge Bay;
Cape Leeuwin (WAM); Hamelin Bay (WAM);
Bunker Bay, Cape Naturaliste (WAM, USNM,
ANSP, MCZ); N side of Cape Naturaliste Light
(AMS, USNM); Busselton (WAM); Duns-
borough (WAM, AMNH); Yallingup Brook
(WAM, ММУ); Yallingup (WAM, ММУ, AMS);
Canal Rocks, S of Yallingup (AMS); Geo-
graphe Bay (AMS); Cape Mentelle, Kil-
carneys (AMS); Bunbury, reef at Capel
(AMS); W side of Carnac Id. (WAM); Rocking-
ham (AMS); Fremantle (ANSP, DMNH,
WAM); near Garden Id., Fremantle (MCZ);

266 HOUBRICK

SW of Garden Id., Fremantle (AMS); Kwinana
(AMS); Dunn Bay (USNM); Swan River
(NMV); Cottesloe (WAM); Carnac Id. (WAM);
Point Peron, Perth (AMNH, WAM, USNM);
Trigg Id. (WAM); Yanchep Reef (WAM); Pal-
linup Estuary (WAM); Port Denison (WAM);
Jurien Bay (WAM); Dongara (AMS); Beach
Colony Shore, Geraldton (MCZ, AMS).

Shell description (Figs. 1-2)—Shell large,
ranging from 60 to 244 тт in length (See
Table 1 for measurements), turreted, elongate,
having apical angle of 25° and teleoconch
of about 25-30 flat-sided whorls that become
weakly inflated or angular on penultimate and
body whorls. Outline of entire spire concave
and early whorls usually missing. Each whorl

FIG. 1. A-F, Shell and operculum of Campanile symbolicum from Hamelin Bay, Western Australia (Western
Australian Museum N4514), 120 mm long, 68 mm wide; operculum 17 mm diameter. A, Apertural view; B,
Side view showing sinuous outer lip; C, dorsal view; D, Anterior view of centrally placed siphonal canal; E,
Free surface of operculum showing subcentral nucleus; F, Attachment surface showing large oval muscle
scar on lower two thirds of operculum; G, Detail of sculpture of early whorls on specimen from Salisbury Id.,
Recherche Archipelago, Western Australia (National Museum, Victoria); H, Holotype of Cerithium leve Quoy
& Gaimard (National Museum of Natural History, Paris, photograph courtesy of Mr. Foubert).

—>
FIG. 2. Campanile symbolicum. а-с, Advanced embryonic shells from egg mass found at Rottnest ld.,
Western Australia (diameter, 0.05 mm); d, SEM of single jaw showing attachment surface (5 mm long); e,
SEM of jaw showing cutting edge (5 mm long); f, Longitudinally cut shell showing apex with calcareous septa
in interior whorls; g, Whole shell cut longitudinally from apex to anterior canal showing whorl configuration
and columella; h, SEM of cross section of jaw, showing four layers, about .055 mm wide. The bottom layer is
the attached portion; i, SEM enlargement of attachment surface of jaw showing microscopic polygonal pits,
each about 7 um long; /, SEM detail of surface periostracum showing cancellate, pitted appearance, 28x; К,
SEM detail of cross section of shell showing, from top to bottom, calcified periostracum with subsurface
tubules, and cross lamellar aragonite, 86x.

267

CAMPANILE ANATOMY AND SYSTEMATICS

vee ee ..00

di, M"

°°208

ХР

Fine

to
qe

‘a AAA
CA
Bun re woe Ñ

vá si

268 HOUBRICK

TABLE 1. Statistical summary of shell measure-
ments of Campanile symbolicum (in mm).

Character Number Range Mean SD
Length 29 60 -244 142.8 50.84
Width 29 21.5-74 44.1 15.81

sculptured with a presutural spiral cord that
produces a weak keel at the base. This spiral
cord is more medianly placed on very early
whorls and may be divided into two spiral
cords on some shells. Early whorls and mid
whorls have a subsutural spiral that tends to
disappear on later whorls (Fig. 1G). Nodules
frequently elongated axially, sometimes en-
tirely absent. Penultimate and body whorls
usually smooth. Below nodules each whorl
sculptured with many microscopic spirally in-
cised lines that are crossed over by numerous
axial, sinuous, growth lines. Suture distinct
and straight. Protoconch (Fig. 2a-c) smooth,
bulbous, about 1% whorls. Protoconch lip
slightly flared at base. Body whorl is round
with the anterior siphonal canal in the center.
Aperture triangular-fusiform and at a 45°
angle to axis of shell. Aperture one-fourth to
one-fifth the length of shell. Interior of aper-
ture glossy white. Anterior siphonal canal dis-
tinct, deep and moderately short, almost
straight but slightly twisted to left of shell axis.
Columella short, concave and twisted slightly
to left at anterior canal. A slight plait appears
at the columella base but does not continue
into the aperture and up the axis of the shell.
Older, larger specimens have an inner
columellar lip, slightly detached from parietal
area. Outer lip thin, sinuous, smooth and with
a deep sinus where attached to body whorl.
Lower portion of outer lip crosses over ante-
rior canal when shell is viewed anteriorly.

A shell cut in half longitudinally, from apex
to anterior canal, exposing the whorl interiors
reveals that the columella is concave through-
out the shell axis and that each whorl is round
in cross section (Fig. 2f,g). Scanning electron
micrographs of cross section of the shell wall
show that it is composed of cross lamellar
aragonite which appears in a wide bottom
layer overlain with looser disordered aragon-
ite (Fig. 2k).

The periostracum of Campanile is unusual
and closely resembles that of some muricid
gastropods such as those in the genus
Aspella Mörch. It is thick and comprises a
cancellate, calcified outer layer and an under-

lying scabrous layer (Fig. 2i,j). Radwin 4
D’Attilio (1976: 245) considered this to be a
chalky white surface layer of the shell and
called it the “intritacalx” but it is simply the
calcified outer portion of the periostracum
(Waller, personal communication), as can be
seen in scanning electron micrographs of the
fractured shell edge (Fig. 2k). In Campanile,
the outer calcified layer of the periostracum
has a cancellate appearance at the surface
that is most clearly seen in young specimens.
Beneath the surface are numerous fine hollow
tubes that run spirally around each whorl. This
layer is fragile and flakes off easily in dried
specimens. In older shells the surface ap-
pears to be pitted and chalky. The pits are
merely depressions formed by the cancellate
pattern in the outer layer. Wrigley (1940: 99)
noted tiny pitted lines on the surface of all
fossil species of Campanile he examined and
| have also seen this pattern on fossils of
Campanile giganteum. This calcified thick
periostracum thus appears to be a character-
istic of the family Campanilidae.

The brown-colored operculum (Fig. 1E-F)
is corneous, moderately thick and paucispiral
with a subcentral nucleus. The operculum has
a straight growing edge and the edge nearest
the nucleus is partially covered with the foot
when the animal is extended. The ovoid at-
tachment scar is on the obverse, bottom two-
thirds of the operculum (Fig. 1F). The oper-
culum diameter is much smaller than that of
the aperture, allowing the animal to retract
deeply into the mid whorls of the shell. In this
retracted state, the operculum fits snugly into
the shell aperture.

Animal (Figs. 3-7)—A brief but accurate
description of the animal was given by Quoy &
Gaimard (1834: 107-108) in the original de-
scription. A more detailed account of the
gross anatomy that centered on the nervous
system but included observations of other
systems was presented by Bouvier (1887a,b),
who compared Campanile with other cerithi-
ids. Although Bouvier’s (1887b) work is ac-
curate and thorough, he failed to describe the
reproductive tract which is essential for an
analysis of comparative relationships among
cerithiaceans. Bouvier's papers were pub-
lished in French journals that were apparently
missed by subsequent authors.

The only figure of a living animal of
Campanile is the one originally given by Quoy
& Gaimard (1833: pl. 54, fig. 2), and it only
shows the head-foot. Part of the foot covers
the edge of the operculum nearest the oper-

CAMPANILE ANATOMY AND SYSTEMATICS 269

cular nucleus. If the shell is cracked, the snail
may withdraw as far as one-half the length of
the shell, causing the edges of the operculum
to fold.

When animals are extracted from their
shells it is apparent that the upper portion of
the visceral mass, comprising the digestive
gland and gonad, does not fill the upper
whorls of the shell apex. These are walled off
by a series of concave, calcareous partitions
or septa and the earliest whorls are totally

filled. The concavity of each septum is adapi-
cal (Fig. 2f-g). Just anterior to the last septum
the shell whorls are lined with a thin brown
membrane. Attached to this membrane is
another thin, transparent, membrane that is
invested with tiny brown spherules of un-
known function. Both of these membranes are
of obvious organic origin and are probably
laid down by the mantle.

The head-foot and mantle edge of live
snails from Point Peron are white to flesh

SSS
—=—— 1

FIG. 3. Campanile symbolicum, removed from shell. A, View of right side о female showing major external
Structures and free part of columellar muscle; B, Left side of animal; C, Cross section of female through mid
mantle cavity showing relationship of major pallial organs. (See Key to Abbreviations, p. 264, for explanation

of lettering.)

270 HOUBRICK

A 10mm

&
14 F N
y Y
г а я
w SS
д

ig р

ip
dsr ppg odg

FIG. 4. Internal anatomy of Campanile symbolicum. A, Female removed from shell with mantle cavity
opened with a lateral-dorsal cut; B, Detail of proximal portion of pallial oviduct showing relationship of kidney,
pericardial sac and seminal receptacle to oviduct. The kidney has been pulled back to expose the proximal
part of the pallial oviduct; C, Diagrammatic representation of sections of pallial oviduct and seminal recepta-
cle showing major anatomical features. Compare with pallial oviduct depicted in drawing A, this figure. (See

Key to Abbreviations, p. 264, for explanation of lettering.)

colored and slightly mottled with light brown
and pink. Extracted snails are small in relation
to their shells. The snout is short, broad and
thick and is conspicuously bilobed at the tip
(Fig. 3B, sn). Tentacles are short and bright
pink, each with a tiny black eye at its broad
base.

Emerging from the exhalant pallial siphon
(Fig. 3A, exs) and running down the right side

of the head-foot, beneath the right eye and
tentacle and down the outer surface of the
foot is a deep ciliated groove (Figs. 3A, 4A,
ctr) in which fecal pellets and other debris are
expelled from the mantle cavity in a string of
mucus. This is probably also used by females
during oviposition. Although | found no evi-
dence of a structure that could be interpreted
as an ovipositor, one associated with this cili-

CAMPANILE ANATOMY AND SYSTEMATICS 271

FIG. 5. A, Dissection of head opened by a dorsal longitudinal cut to expose anterior alimentary tract.
Connective tissue surrounding nerve ring has been removed. Subesophageal ganglion hidden beneath
mid-esophagus. B, Stomach opened by a dorsal longitudinal cut. Arrows indicate direction of ciliary currents.
(See Key to Abbreviations, p. 264, for explanation of lettering.)

ated groove may develop during the spawn-
ing season.

The foot is moderately small in relation to
the shell and has a whitish sole with slight
traces of yellow. Quoy & Gaimard’s (1834:
107) observations on the color of animals
from King George Sound agree with mine.
They noted that the underside of the foot was
yellowish and striated. | did not see striations
in the Point Peron specimens. The entire
edge of the sole has a deep ciliated glandular
furrow (Fig. 3B, cf) that appears to be a pedal
gland. It produces mucus, but it was not de-
termined if the gland cells were epithelial or
subepithelial. The foot is capable of contrac-
tion into numerous, compact transverse folds
that appear to secrete mucus in living ani-
mals. It is powerful enough to pull the heavy
shell enabling animals to partially burrow and
even crawl up rocky surfaces.

The large columellar muscle (Fig. ЗА-С,
cm) is very long, comprising 2-3 whorls in a
retracted animal. This muscle is white and
thick anteriorly but flattens and tapers rapidly

near its proximal origin on the columella of the
shell.

Posterior to the mantle cavity is the visceral
mass of 6-7 whorls that consists of a large
two-lobed kidney (Fig. 3A, k), a long stomach
(Fig. ЗА, st) of 1% whorls and a digestive
gland-gonad complex (Fig. 3A, dg). The latter
has a distinctive banded appearance, clearly
seen in both living and preserved snails: at
the periphery of each whorl it is light gray
while the inner surfaces of the whorls are
darker brown, spotted with gray and overlain
by a ramose network of white calcium.

The digestive gland is dark brown and is
slightly overlain by the gonad in mature ani-
mals. Ovaries are externally yellow and con-
sist of tiny spherules located along the pe-
riphery of the whorls. The testis is not as easi-
ly differentiated from the digestive gland ex-
cept for a change of external texture along the
periphery of the whorl. | did not observe ani-
mals during their peak reproductive season;
consequently ripe snails may have more
conspicuous, characteristic gonads. Gonads

272 HOUBRICK

are discussed in more detail in the section on
the reproductive tract.

Mantle cavity and associated organs (Figs.
3—4). The mantle cavity is wide and deep. At
the base of the left side is a large brown, oval-
shaped, bipectinate osphradium (Fig. ЗВ-С,
os; Fig. 4A, os) directly adjacent to the cteni-
dium. It begins behind the distal end of the
ctenidium and closely resembles it in overall
morphology, except that the leaflets are wider
and more oval. It is referred to by Bouvier
(1887b) as the “fausse branchie.” It runs
parallel to the ctenidium but does not extend
the length of the mantle cavity as in other
cerithiaceans. The osphradium is slightly ele-
vated from the mantle skirt on a central axial
ridge that bears a series of numerous, flat,
bipectinate leaflets. Each of these is attached
to the stem of the axis and also fused basally
to the mantle skirt. Histological sections show
that each leaflet has an external morphology

of numerous parallel ridges that run dorso-
ventrally or vertically to the osphradium axis.
Cross sections reveal a surface structure
covered with ciliated cells and more numer-
ous darkly-stained cells.

The typically monotocardian ctenidium (Fig.
3B, ct; Fig. 4A, ct) is pink and extends most
of the length of the mantle cavity to end a
short distance from the inhalant pallial siphon.
A large, white efferent branchial vessel (Fig.
4B, ebv) lies along the basal length of the left
side of the ctenidium.

The thick mantle edge is weakly bilobed,
flared and has a slightly scalloped appear-
ance. It consists of an inner row of tiny papil-
lae found only on the upper two thirds of the
mantle edge and an outer, continuous, scal-
loped border (Fig. 3A-B, mp). The scallops
are larger on the ventral part of the mantle
edge. The deep groove between the two man-
tle lobes secretes the shell but also traps

FIG. 6. SEM micrographs of radular ribbon of Campanile symbolicum. A, View of central portion of radula
showing relationship of various taenioglossate teeth. Radular ribbon is 8.2 mm long and 2.15 mm wide; B,
Detail of lateral and marginal teeth, showing tiny cusps adjacent to large cusp of lateral tooth and smooth
outer surfaces of inner and outer marginal teeth; C, Enlargement of half row of radular ribbon with marginal
teeth folded back showing their insertion on underlying radula membrane; D, Detail of rachidian teeth

showing basolateral projections.

CAMPANILE ANATOMY AND SYSTEMATICS 273

FIG. 7. Histology of reproductive and alimentary tracts. A, Transverse cross section of seminal receptacle,
showing network of tubules. Note villous walls of empty tubules at top and smooth walled chambers
containing sperm at bottom; B, Longitudinal cross section of seminal receptacle showing connection of
tubules; C, Oblique section of seminal receptacle showing opening of duct (osr) leading from seminal
receptacle to pallial oviduct; D, Detail of sperm filled chamber in seminal receptacle showing spermatozoans
with dark heads (H) oriented along wall of chamber (RW) and flagella (F) projecting into chamber lumen; E,
cross section of mid esophagus showing shallow folds in esophagus wall. The lumen (les) is filled with
detritus. Note mass of connective tissue (cnt) and thin muscular layer (ml) surrounding esophagus; F, Cross
section of esophageal pouch showing deeply folded walls and opening into esophagus (OES).

274 HOUBRICK

debris and moves particles by ciliary action
from between the mantle and shell. The in-
halant siphon (Fig. 3H, ins) is thick and com-
prises a slight fold in the mantle wall, but is not
well marked in contrast to the thicker exhalant
siphon (Fig. 3A, exs).

The hypobranchial gland (Fig. ЗА-С, hg;
Fig. 4A, hg) is a large organ, about 6 тт
wide, pinkish-tan in color that extends the
length of the mantle cavity where it lies be-
tween the ctenidium and intestine. It partially
covers one half of the intestine, longitudinally,
in a thick sheet. The hypobranchial gland be-
gins immediately behind the exhalant pallial
siphon and is thus the most anterior of all pal-
lial organs. Its surface is composed of numer-
ous transverse ridges or folds which are papil-
late along their edges, and most numerous
and thin at the rear of the mantle cavity. They
become progressively thicker toward the
anterior of the snail. The ridges are flocculent
in texture and easily fall apart when touched
with a probe. The papillate ridges of the hypo-
branchial gland adjacent and anterior to the
anus are thicker and extended into numerous,
tiny, flat leaflets (Fig. 4A, /hg). The gland in
this region is thicker and appears to be slightly
different in texture. In cross section, it is sepa-
rated from the posterior part by a band of tis-
sue that is part of the siphonal musculature.
Sections show that it consists mainly of
elongate goblet cells and it may produce ad-
ditional mucus used in conjunction with the
exhalant siphon. Its exact function is uncer-
tain. Sections of the hypobranchial gland
show that it is composed of elongate, multi-
vacuolated goblet cells that are attached to a
basal membrane adjacent to the circular
muscular tissue of the mantle wall. Most of the
vacuoles appear empty in fixed tissue but
some are filled with tiny, darkly stained gran-
ules.

The rectum (Figs. 3A, 4A, r) is a long, dark
brown tube, about 3—4 mm thick that lies be-
tween the hypobranchial gland and pallial
gonoduct ending near the exhalant siphon.
The anal opening (Fig. 4A, a) is surrounded
by tiny papillae.

The pallial gonoducts lie to the right of the
intestine, are open and comprise two laminae
which are highly glandular, especially in the
female.

Alimentary tract.—The alimentary system
of Campanile is slightly different from that of
most cerithiaceans. One of the notable fea-
tures is a short, wide, bilobed snout (Fig. 4A,
sn) that was noted by Bouvier (1877a, b) as a

distinguishing character. The mouth lies at the
tip of the snout, recessed between the two
lobes that comprise the snout apex. The
snout area and head are thick and very
muscular.

A pair of large, thick, semilunar-shaped
jaws (Fig. 5A, /) that are yellowish brown in
color and about 5 mm long are inserted in the
upper lateral walls of the anterior end of the
buccal cavity. The jaws are superficially
smooth except for their irregular cutting edges
that appear to be formed of numerous trans-
verse rods (Fig. 2d-e). Scanning electron
micrographs of the jaws reveal a complex
ultrastructure. The free surface of each jaw,
exclusive of the cutting edge, is generally
smooth but shows concentric lines of growth
radiating from the base where the jaw is in-
serted in the wall of the buccal cavity. The
attached surface of each jaw is made up of
many microscopic polygonal pits (Fig. 2).
Each pit is about 7 ит in length and its poly-
gonal walls probably conform to individual cell
boundaries. Each pit is perforated with nu-
merous tiny holes. The cutting edge of a jaw
comprises a matrix of many thin, transverse
rod-like structures. In cross section, a jaw is
composed of four consecutive layers (Fig.
2h). At the smooth surface is a wide layer of
transverse rods and beneath this is another
thin layer of transverse rods. Another thin,
nondescript layer follows and beneath this a
final thick layer of smooth material. It is this
final layer that is attached to the wall of the
buccal cavity and has the pitted surface. The
growing surface of the jaw appears to be the
concave portion opposite the cutting edges.
The functional significance of the complex
ultrastructure of the jaws was not deter-
mined.

The buccal mass (Fig. 5A, bm) is spherical
and attached to the walls of the buccal cavity
by numerous tensor muscles that insert onto
its entire surface. These are more numerous
laterally and ventrally. The odontophoral
cartilages (Fig. 5A, od) are very large and
thick.

The radula (Fig. 6A-D) is stout, moderately
short and wide, and about one-tenth the
length of the shell. Two radular ribbons from
animals with shells about 100 mm in length
averaged 8mm long, 2.25mm wide and
comprised 43 rows of teeth. The rachidian
tooth is straight and has a large, plate-like cut-
ting edge comprising a large, broad, triangu-
lar cusp flanked on each side by a single, tiny,
blunt denticle. The lateral tooth (Fig. 6B-C) is

CAMPANILE ANATOMY AND SYSTEMATICS 275

trapezoid in shape, and has a basal plate with
a slight median bulge and a long lateral ex-
tension that attaches to the basal membrane.
The top is slightly concave and has a cutting
edge comprising one small, sharp denticle, a
large, platelike triangular, sharp cusp and one
to two tiny blunt denticles, consecutively from
the inner side. The marginal teeth (Fig. 6B-C)
are stout, curved and hook-like with sharp tips
and a single denticle on the upper, inner side
of each tooth. The bases of the marginal teeth
are spatulate where they attach to the basal
membrane.

Two yellowish, spherical, loosely-compact-
ed salivary glands (Fig. 5A, sg) lie anterior to
the nerve ring and lateral and dorsal to the
origin of the esophagus. The glands lie close
against the nerve ring but do not pass through
it. Externally, each of these glands appears to
be composed of a matrix of fine tubules. No
salivary ducts leading to the oral cavity are
visible in gross dissections. Sections of the
salivary glands stained blue with Harris’
hematoxylin reveal numerous fine tubules
comprised of dark-staining secretory cells and
lighter, more numerous, highly vacuolated
mucoid cells. A salivary duct is embedded in
the lateral portion of each gland, adjacent to
the buccal mass. The exact point of entry of
the salivary ducts into the oral cavity was not
determined, but is probably in front of the
nerve ring.

Anterior and adjacent to the nerve ring and
emerging laterally at the base of the salivary
glands is a pair of small, darkly-colored, lobate
buccal pouches (Fig. 5A, bp). They are con-
nected to the buccal cavity and lie dorso-
laterally to it. The buccal pouches are com-
posed of muscular tissue and internally each
cavity is highly folded and lined with non-
ciliated tissue that comprises a large surface
area of tightly packed, dark-staining cells filled
with many dark granules (Fig. 7F). Beneath
this layer of cells is another layer of more
loosely packed cells with simple nuclei that
stain pink with Eosin Y indicating an abun-
dance of cytoplasm. The histology (Fig. 7F) of
the buccal pouches differs markedly from that
of the buccal cavity and anterior esophagus.

Cross sections of the anterior esophagus
reveal a deep dorsal food channel and two
deep, ventrolateral channels which are а!
highly folded longitudinally and lined with long
cilia. Most of the cells lining the remainder of
the anterior esophagus are not ciliated but
elongate and goblet-shaped.

At the point where the anterior esophagus

becomes the mid-esophagus (Fig. 5A, me)
the body cavity is divided by a thin transverse
septum lying directly behind the nerve ring.
This septum is closely associated with the
many muscular elements of the posterior
buccal mass and walls of the buccal cavity. It
was not clear if this septum completely di-
vides the cephalic hemocoel as does the
transverse septum of trochaceans. Its func-
tion and exact relationship to the cephalic
hemocoel remain uncertain. As the anterior
esophagus passes through the nerve ring the
food channel and grooves become highly
folded and the dorsal food channel seems to
disappear directly behind the nerve ring at the
point of torsion.

The mid-esophagus is a wide, dorso-
ventrally flattened tube that, in comparison
with the anterior esophagus, has few longitu-
dinal folds or grooves. The ventral portion of
the mid-esophagus is smooth while the dorsal
and lateral parts have 4—6 shallow depres-
sions (Fig. 7E). The histology of the mid-
esophagus is identical to that of the anterior
esophagus only there are more ciliated col-
umnar epithelial cells. The mid-esophagus is
buried in a large mass of loosely compacted
connective tissue (Fig. 5A, cnt) which begins
immediately behind the nerve ring where it is
thickest. It gradually tapers posteriorly and be-
comes concentrated to the left of the esopha-
gus. Cross sections of the mid-esophagus
show that a thin layer of loose connective tis-
sue (Fig. 7E, cnt) surrounds the mid-esopha-
gus for its whole length and it is surrounded by
a very thin muscular layer (Fig. 7E, ml) which,
in turn, is enveloped in more loose connective
tissue. The esophagus is thus surrounded by a
double layer of connective tissue which histo-
logical sections show has no connection or
relationship to the interior esophagus. The
function of this thin muscular membrane and
its relationship to the esophagus and sur-
rounding connective tissue is unknown.

The posterior esophagus is oval to round in
cross section, and the wall is folded longi-
tudinally. The interior surface is ciliated, and
made up of elongate columnar epithelial cells
and few mucus cells.

The stomach (Fig. 5B) occupies 172 coils of
the lower visceral mass and differs markedly
from those of other cerithiaceans | have ex-
amined in several features. It is a complex
structure and difficult to interpret, functionally.
Although a style sac (Fig. 5B, ss) is present at
the intestinal end of the stomach, there is no
crystalline style. Freshly collected specimens

276 HOUBRICK

| dissected had no trace of a style in their
stomachs, but a normal fecal rod or protostyle
was present and led into the intestine.
Campanile lacks a cuticular gastric shield that
one sees in other cerithiaceans. Instead there
is an elongate raised, non-cuticular muscular
area (Fig. 5B, gs) and a very complex
grooved sorting area (Fig. 5B, gsa) lying
adjacent to the esophageal opening at the
middle of the stomach. The largest portion of
the raised muscular area is probably homolo-
gous to the area supporting the gastric shield.

If the stomach is opened by a dorsal longi-
tudinal cut, the posterior esophagus (Fig. 5B,
eso) is seen to open into the stomach at its left
mid-section through a circular sphincter mus-
cle. Food passing into the stomach is immedi-
ately directed to a large sorting area marked
by many latitudinal folds (Fig. 5B, sa). From
here it moves to a deep grooved channel (Fig.
5B, gsa) and into a deep pit lined with glandu-
lar tissue that is folded into spirally arranged
leaflets (Fig. 5B, s/). There are about five
major leaflets at the top of the sorting area
and many smaller ones leading to the base of
the pit. Each leaflet is further folded into longi-
tudinal ridges on each of its sides. The bases
of the leaflets are smoother and have fine
longitudinal grooves. Ciliary currents move
down the longitudinal folds and grooves to the
base of each leaflet and thence deeper into
the muscular pit of the sorting area. The base
of the pit is blind. In the pit of the sorting area
are found larger particles and sand grains up
to 1.5 mm in diameter.

After sorting, food is probably transferred to
the posterior portion of the stomach. This
large, white, tapering sac-like area (Fig. 5B,
sc) lies at the rear of the stomach and is lined
with fine transverse folds within which food
particles are rotated. The area is probably a
vestige of the spiral caecum. Emerging from
the caecum is a large flat fold (Fig. 5B, ff). At
the base of the “gastric shield” is a deep
groove leading to the digestive gland (Fig. 5B,
Id). The muscular walls of the caecal area are
thick and internally consist of loose connec-
tive tissue interlaced with thousands of fine
fibrous muscle strands. Anterior to the large
muscular area or gastric shield is a deep
ridged groove that leads into the style sac and
is bordered at its left by the major typhlosole
(Fig. 5B, t,) and on its right by the minor
typhlosole (Fig. 5B, 45). The style sac is es-
sentially a smooth area bisected by the major
typhlosole and food groove (Fig. 5B, fg) lead-
ing into the intestine (Fig. 5B, int). Tiny, ovoid,

fecal pellets found in the intestine and rectum
are held in a fine mucous strand.

Excretory system. The kidney. (Fig. ЗА-В,
k) is a large dark brown organ, about 1.5
coils in length. It overlays the end of the man-
tle cavity and covers part of the albumen
gland and much of the pericardium. As it
nears the stomach it tapers rapidly and is less
thick. The under surface of the kidney is cov-
ered by the thin mantle through which may be
seen the renal lamellae (Fig. 4B, rl). The kid-
ney opening (Fig. 48, ko) is a small slit lo-
cated at the anterior end near the pericardium
and faces the mantle cavity. Another small
opening, the renopericardial duct (Fig. 4B,
rpd), leads from the kidney into the pericardial
sac. The part of the kidney bordering the peri-
cardium is lighter in color and looks like a
nephridial gland, but sections of this part of
the kidney do not show any cellular differ-
ences.

An area of distinctive tissue lies adjacent to
the rear of the main part of the kidney and
extends over the anterior portion of the stom-
ach. It is of a different structure and texture
from the kidney and is deeply embedded
around the style sac of the stomach. The in-
ternal structure is a tubular matrix of fine tiny
sacs that are filled with yellowish concretions
that are probably waste.

Nervous system. Bouvier (1887b: 149) has
described this in great detail and presented
accurate figures of it (Bouvier, 1887b: pl. 8,
fig. 33). His drawings are difficult to interpret
at first glance because he shows the nerve
ring with the cerebral commissure cut and the
cerebral ganglia reflected back to expose the
pleural and subesophageal ganglia.

The cerebral ganglia (Fig. 5A, /cg, rcg) are
above the esophagus posterior to the buccal
mass. They are large, elongate and joined by
a long cerebral commissure. Four primary
nerves emerge anteriorly from each cerebral
ganglion and three others run into the walls of
the buccal cavity. These innervate the lips,
tentacles and eyes and the fourth is the con-
nective to the buccal ganglion (Fig. 5A, bg).
Each of the pleural ganglia (Fig. 5A, /pg, rpg)
are joined to the cerebral ganglia by very dis-
tinct, different connectives. The right pleural
ganglion (Fig. 5A, rpg) lies close to the right
cerebral ganglion and is joined to it by a short,
thick connective. The left pleural ganglion dif-
fers in lying farther away from the left cerebral
ganglion and is joined to it by a long slender
connective. A large left pallial nerve (Fig. 5A,
рп) emerges from the left pleural ganglion

CAMPANILE ANATOMY AND SYSTEMATICS 277

and runs into the body wall. А long supra-
esophageal connective (Fig. 5A, sec)
emerges from the right pleural ganglion,
passes over the esophagus and runs into the
left body wall where it enlarges to form the
supraesophageal ganglion (Fig. 5A, seg).
This is connected to the left pallial nerve by a
moderately long dialyneury. The two pedal
ganglia are joined to the cerebral and pleural
ganglia by long slender connectives. The
pedal commissure is slender and of moderate
length. Although | did not see any statocysts,
Bouvier (1887b: 149) described them as lying
at the posterior base of the pedal ganglia and
noted that each statocyst contained numer-
ous statoliths.

At the base of the left pleural ganglion lies
the subesophageal ganglion. The connection
between these two ganglia is very short and
thick and it is difficult to separate the two. The
subesophageal ganglion is joined to the right
pleural ganglion by a thick zygoneury. There
is a long visceral nerve that runs to the vis-
ceral ganglia and a typical visceral loop is
present.

In summary, the cerebral, pedal and left
cerebral-pleural connectives are long, slender
and contribute to a “loose” state of the nerve
ring. In contrast, condensation of the nerve
ring is achieved by the close connection be-
tween the left pleural and the subesophageal
ganglia, the short, thick connective between
the right cerebral and pleural ganglia, and the
dialyneury between the pleuro-supraesopha-
geal ganglion and left pallial nerve.

Reproductive system. Males and females
have open pallial gonoducts and males are
aphallic. The pallial gonoducts of both sexes
are relatively simple and their open condition
is best visualized as a slit tube running the
length of the mantle cavity, forming dorsal and
ventral lobes with the slit facing the mantle
cavity. Each lobe comprises an inner and outer
lamina (Fig. ЗС, il, ol; Fig. 4C, il, о!) fused
together along their axes to the mantle wall.
The inner lamina is also fused on its right side
to the mantle while the outer lamina is mostly
free except for its fused axis. Both laminae
are lined internally with numerous transverse
glandular folds.

Campanile may be a protandric herma-
phrodite because both sexes have a seminal
receptacle. This is discussed in more detail
later in this paper.

The female pallial duct is larger and more
glandular than that of the male. At its proximal
left end is an opening that leads to a sac-like

seminal receptacle (Fig. 4B, sr) which is unus-
ually placed in that it bulges into the pericardial
sac (Fig. 4B, ps) although it is histologically
distinct from it. The seminal receptacle (Fig.
4А-С, sr) is usually a single compact sac but
may have several lobes. The interior is a
branching series of villous tubes converging
at the base of the receptacle (Fig. 7B) to form
a single duct that opens to the distal pallial
oviduct near the beginning of the albumen
gland (Fig. 7C, osr). Sections of the seminal
receptacle show that the columnar epitheli-
um (Fig. 7B) is ciliated. Sperm are stored in
the tubes (Fig. 7A) with the heads (Fig. 7D, H)
oriented in the walls (Fig. 7D, RW) and their
flagella (Fig. 7D, FL) projecting into the lumen
of the tubes. Some tubes did not contain
sperm and are more villous than others, as
may be seen in a cross section of the recepta-
cal (Fig. 7A, top portion; C, ctb). These may
function as a bursa.

The pallial oviduct (Fig. 4C) has no sperm
collecting gutter, no bursa or spermatophore
receptacle and no tubes in the walls of the
laminae. The inner surface of each lamina is
thrown into transverse folds along its entire
length. These folds become yellow, thin,
broadly laminate at the proximal end of the
oviduct and constitute the albumen gland
(Fig. 4A, C, ag). Bouvier (1887b: 147), una-
ware that this was part of the pallial gonoduct,
remarked that this area resembled gill leaf-
lets. These leaflets secrete copious amounts
of albumen when stimulated. Sections of the
albumen gland show large cells with little
nuclear material and large vacuoles. The mid
(Fig. 4A, gil) and distal parts of the pallial
gonoduct differ from the albumen gland in
having a thick outer lamina of white glandular
tissue and probably give rise to the gelatinous
portion of the spawn mass. The base of the
open oviduct (Fig. 4A, С, odg) is lined with fine
transverse folds and is densely ciliated. The
entire wall of the outer lamina has a median
longitudinal furrow (Fig. 4C, do/), where the
thickness of the wall is reduced so that the
free half can be folded over the inner lamina
like a baffle to form a physiologically closed
tube as in other prosobranchs with an open
duct (Fig. 3C, 4C, b). The inner lamina is
fused on its right side to the body wall and
appears comprised of thick, irregular glandu-
lar folds on its inner functional surface (Fig.
4A, gil).

The male pallial gonoduct is a thinner, more
simple open duct and is highly glandular only
at its proximal end where it probably functions

278

as а prostate. The inner lamina is fused on its
left side to the body wall as in the female. An
opening to a small seminal receptacle occurs
in the proximal left end of the pallial gonoduct
and leads to a sac-like receptacle that lies
within the pericardial sac. It appears to be
morphologically identical to the female
seminal receptacle. Remains of what ap-
peared to be a disintegrating spermatophore
were found in the female oviducal groove;
thus, the male pallial gonoduct may also
secrete spermatophores, but this needs con-
firmation. Sections through the testis show
typical seminiferous tubules filled with various
stages of developing spermatozoans. Sperm
extracted from the vas efferens were all
eupyrene but my specimens were taken
in early winter; thus, spermic dimorphism
should be looked for more closely in spring
during the height of the reproductive season
when animals are seen pairing.

REPRODUCTIVE BIOLOGY

The head-foot region of sexually mature
snails becomes pink when they are ripe. This
is especially marked in females whose ova-
ries and eggs are also the same color. The
significance of this color in the head-foot is
unknown. Pairing was not observed but de-
position of spawn begins in September and
lasts throughout November (Dr. Robert Black,
personal communication). Spawn masses are
attached to marine angiosperm grass blades,
macroalgae, rocks or other objects on the
substratum and are frequently cast up on the
beach. Spawn masses seem to be neutrally
buoyant.

Eggs are deposited in large jelly-like, cres-
cent-shaped spawn masses (Fig. 8A-B), and
closely resemble the spawn of opistho-
branchs. An average spawn mass is 175 mm
in length, 21 тт wide and 5 тт thick, and
contains about 4,000 pink eggs (Table 2). A
spawn mass is transparent, free of debris on
its surface and viscous throughout. The at-
tachment surface is opaque (Fig. 8A, as) and
is located at the base of the mass, usually at
one end. The outer covering is very thin,
parchment-like and has tiny longitudinal stria-
tions. Within the jelly mass the egg capsules,
joined by chalazae, appear as a continuous
spirally coiled strand (Fig. 8B). There is ап
average of three eggs per capsule (range 1-
5), each about 0.5 mm in diameter. It was not
determined if any of the eggs functioned as
nurse eggs.

HOUBRICK

FIG. 8. Spawn of Campanile symbolicum. A, Indi-
vidual spawn mass showing attachment surface
(as), 117 mm long; B, Detail of jelly strands and eggs
composing spawn mass.

TABLE 2. Statistical summary of spawn measure-
ments of Campanile symbolicum (in mm).

Statistic

n=5 Mean Range SD
Length 120.2 78-240 66.77
Width 22.4 18-75 2.96
Thickness 4.7 3.8—6.5 1.13
Number of
Embryos 4025 3000-6624 1484.2

Embryonic stages ranging from early
cleavage to advanced veligers are present
within a single spawn mass. Advanced veliger
stages have black eyes, small velar lobes,
and the embryonic shells (Fig. 2а-с) are
smooth, comprise 1% whorls and lack a
sinusigera notch, so typical of mainly plank-
tonic larval shells. A free veliger is unknown,
but the advanced state of the late veliger
stages and the embryonic shell suggest direct
or a short demersal development. Growth of
newly hatched snails is rapid (Robert Black,
personal communication), but nothing is
known of the age of adult snails.

CAMPANILE ANATOMY AND SYSTEMATICS 273

ECOLOGY

Campanile symbolicum normally occurs
subtidally in large populations on sandy
patches between rocks on limestone reefs.
The substratum may have seagrass, macro-
algae or may be predominantly sandy. The
species is sometimes found in the intertidal
zone but the bulk of the population is subtidal.
At Pt. Peron, Western Australia, | observed a
large population at a depth of 3 m. Animals lie
on the sand, sometimes slightly buried, or
adjacent to rocky shelves where they are fre-
quently found jammed together. They appear
to be inactive during the day with only a few
traces in the sand to indicate movement. The
species is probably nocturnal because ani-

mals kept in an aquarium were active mostly
at night. Campanile shells have numerous
Hipponix conicus (Schumacher) attached to
their last two whorls. These are usually on the
base of the body whorl adjacent to the siphon
or on the outer lip.

The outer lip of adult Campanile shells is
thin and frequently broken. Crustacean pred-
ators can peel back the lip only a short way
because it becomes very thick on the penulti-
mate whorl and resists breakage. Moreover,
the animals can retract deeply into their shells
and thus appear to be safe from predators. No
drilled shells were seen.

Fossil records.—Campanile symbolicum
occurs as a fossil in the Pliocene (George
Kendrick, personal communication) and in the

FIG. 9. Geographic distribution of Campanile symbolicum.

280 HOUBRICK

early Pleistocene (Ludbrook, 1971) of the
Eucla Basin of South Australia, although most
workers now consider the Eucla Basin to be
late Pliocene (Ponder, personal communica-
tion). The Pliocene fossil, Telescopium gigas
Martin, 1881 from Java is very similar to
Campanile symbolicum and is either con-
specific with it or a close relative.

Geographic distribution.—Confined to
southwestern Australia.

SYSTEMATICS

Superfamily Cerithiacea Fleming
Family Campanilidae Douville, 1904

Diagnosis.—Shell large with chalky sur-
face, elongate, turreted, with straight-sided or
slightly convex whorls and moderately incised
suture. Body whorl wide and truncate. Growth
lines sinuous. Sculpture of suture cords and
nodes frequently absent or weak. Aperture
narrow and fusiform, anterior canal of moder-
ate length, columella smooth or plaited, peri-
ostracum chalky. Operculum ovate, corne-
Ous, paucispiral and with eccentric nucleus.
Radula taenioglossate, sexes separate,
males aphallic, pallial gonoducts open.

Remarks.—Shell characters, the radula,
operculum and open pallial gonoducts of both
sexes point to the superfamily Cerithiacea as
a proper assignment for this group.

The family Campanilidae was proposed by
Douvillé (1904: 311) who later, without ex-
planation, transferred the genus Campanile
back to the family Cerithiidae Fleming
(Douville, 1928: 9) and finally regarded it as a
subgenus of Cerithium Bruguiére (Douvillé &
O’Gorman, 1929: 362). Most subsequent ac-
counts have ignored the family name and
have generally placed Campanile in the
Cerithiidae. Thiele (1931: 215), Wenz (1940:
771) and Franc (1968: 281) recognized the
group as a subfamily, Campanilinae, in the
Cerithiidae. Anatomically, Campanile sym-
bolicum cannot be referred to the family
Cerithiidae and does not fit the limits of any
other cerithiacean family. | believe familial
Status is justified for this group on the basis of
a coherent lineage seen in an extensive fossil
record, a unique shell structure and physi-
ognomy, and the distinctive anatomical char-
acters described in detail in this paper.

Genus Campanile Fischer, 1884

Type-species: Cerithium giganteum
Lamarck, 1804 [Eocene] (by subsequent
designation, Sacco, 1895: 37).

Synonymy

Campanile “Bayle” in Fischer, 1884: 680;
Sacco, 1895: 37; Douvillé, 1904: 311;
Cossmann, 1906: 71; 1908: 19-27;
Boussac, 1912: 19; Iredale, 1917: 325 (in
part); Delpey, 1941: 3-5; Cox, 1930: 148-
150; Wenz, 1940: 771; Andrusov, 1953:
452; Franc, 1968: 282.

Ceratoptilus Bouvier, 1887a: 36 (type-spe-
cies, by monotypy, Cerithium leve Quoy &
Gaimard, 1834); 1887b: 146, pl. 8, fig. 33;
pl. 9, fig. 38 (in part).

Campanilopa lredale, 1917: 325-326 (ге-
placement name for Campanile, to be ap-
plied to fossil species only) (т part);
Delpey, 1941: 20.

Diagnosis.—Shell large, turreted, elongate
and with straight-sided whorls or slightly con-
vex whorls and moderately incised suture.
Body whorl sharply truncate. Shell with
chalky, cancellate outer periostracum that
forms a microscopic, pitted surface. Growth
lines sinuous. Aperture narrow, fusiform, and
at a 45° angle to shell axis. Anterior siphonal
canal moderately long, twisted slightly to left.
Outer lip thin, smooth and sinuous with an
anal notch. Base of outer lip extends over
anterior siphonal canal. Columella smooth,
concave. Shell sculpture of early whorls com-
prised of spiral cords and spiral rows of
nodules; later whorls usually smooth. Proto-
conch smooth, 22 whorls. Operculum ovate,
corneous, paucispiral with eccentric nucleus.
Radula taenioglossate (2+1+1+1+2).
Sexes separate, males aphallic, pallial gono-
ducts open, albumen gland large, seminal
receptacle projected into pericardium. Spawn
comprised of jelly-like strings with large eggs.
Ctenidium monopectinate, osphradium short,
bipectinate. Pair of salivary glands in front of
nerve ring. Stomach complex, without style.
Nervous system zygoneurous. Commissures
of nerve ring long.

Remarks.—The type-species of this taxon
has been the subject of debate. Campanile
was originally proposed to accommodate a
mixed group of large cerithiid-like snails. The
name Campanile was proposed as a sub-

CAMPANILE ANATOMY AND SYSTEMATICS 281

genus of Cerithium by Fischer (1884: 680),
who credited the name to Bayle. Fischer’s
diagnosis was based mainly on conchological
characters derived from both the fossil spe-
cies and from the Recent one, because the
operculum is mentioned. Although this diag-
nosis mentioned the living species first (cited
as Cerithium laeve) and then cited Cerithium
giganteum Lamarck, 1804 as a fossil ex-
ample, a type-species was not designated.

Douvillé (1904: 311) regarded the genus
Campanile as sufficiently distinct from other
cerithiaceans to comprise a separate family
and cited Cerithium laeve Quoy & Gaimard (=
Campanile symbolicum lredale) as repre-
sentative of the family.

Cossmann (1906: 72), who considered
Campanile to be a subgenus of Cerithium
Bruguiére, apparently unaware of Sacco's
(1895) prior designation of a type-species,
selected Cerithium giganteum Lamarck. Cox
(1930: 148) cited Cossmann’s (1906) desig-
nation and most other authors have errone-
ously attributed the selection of the type-spe-
cies to Cossmann.

Most of the large Tethyan species are
characterized by shells with columellar plaits
that extend along the entire axis: of the shell
and have a more nodulose sculpture. In con-
trast, the living species and a Pliocene fossil,
Cerithium gigas (Martin, 1881), lack these
characters. Cossmann (1906), noting this dif-
ference as well as other sculptural and aper-
tural ones, doubted that the living species and
its Pliocene fossil homologue from Java
should be included together in the same
group. He pointed out that there were no fossil
representatives of Campanile known from the
Miocene, implying a broken lineage. He did
not, however, propose a new generic name
for the group without plaits.

The living species, Campanile symbolicum
was subsequently referred to the genus
Telescopium Schumacher by Sowerby (1865;
cited as Cerithium laeve), who noted that
there were essential differences between it
and the fossil, Cerithium giganteum Lamarck
(cited as Cerithium gigas, probably in error for
giganteum because the name gigas was pro-
posed in 1881 for a different fossil species).

The soft parts of Campanile symbolicum
were described by Bouvier (1887a: 36; cited
as Cerithium laeve Quoy & Gaimard), who
realized that this species is anatomically very
different from animals in the genera Cerithium
and Telescopium; consequently he proposed

the genus Ceratoptilus to accommodate it.
Bouvier (1887a, b) was obviously unaware
that the name Campanile Fischer, 1884, was
available. He included the Tertiary fossils in
his new genus.

Iredale (1917: 325), also unaware of Sacco's
(1895) designation of Cerithium giganteum
Lamarck as the type-species of Campanile,
did not accept Cossmann’s (1906) designa-
tion of this taxon as type-species. Iredale
(1917) believed that the name Campanile
should be restricted to the living species be-
cause the original diagnosis of Fischer (1884)
employed opercular characters. He stated
that Cerithium giganteum Lamarck could not
be regarded as congeneric because it was, in
his opinion, much more like Terebralia Swain-
son, 1840 “in every essential shell character.”
Iredale (1917) thus excluded the fossil spe-
cies from Campanile and proposed the genus
Campanilopa for them. It should be noted that
Iredale’s opinion regarding the type-species is
incorrect: had Sacco (1895) not already de-
signated a type-species, Cossmann’s (1906)
designation of Cerithium giganteum Lamarck
would be correct, Iredale’s (1917: 325; 1949:
20) opinions notwithstanding. The name
Campanilopa lredale, 1917, which Iredale
applied to the large Tethyan fossils, thus be-
comes a junior synonym of Campanile.
Campanilopa was regarded as a subgenus of
Campanile by Delpey (1941: 21) for those
fossil species that have columellar plaits.
Iredale (1917) was unaware that some of the
Tertiary species had smooth columellas and
were very much like the Recent Campanile
symbolicum.

Boussac (1912: 22-23), noting Coss-
mann’s (1906) suggestion that Cerithium
laeve was probably essentially different from
the large fossil Campanile species, carefully
examined the shells of both groups. He found
no essential differences between the Recent
species and the fossils and concluded that
they were congeneric and should both be as-
signed to Campanile. He did not consider
Campanile to constitute a family.

Wrigley (1940: 111) concurred with
Boussac (1912) and regarded the English
Eocene fossil Campanile species to be con-
generic with the Recent species, Campanile
symbolicum, from Australia. He was соп-
vinced that the sculptural differences did not
warrant a generic separation.

Iredale (1949: 20), in a short note, dis-
agreed with Wrigley (1940) and stated that

282 HOUBRICK

examination of a series of specimens from
Australia convinced him that the Recent spe-
cies had “nothing whatever to do with the
British Eocene fossils.” He suggested that the
fossils were probably distantly related to the
genus Terebralia Swainson, 1840.

Delpey (1941) wrote the most comprehen-
sive paper on Campanile and presented a
thorough history of the nomenclature, tracing
the fossil lineage of the group. She delineated
the generic characters of Campanile and
showed that there is considerable interspecific
variation in the presence, placement and num-
ber of columellar and parietal plaits as well as
in shell sculpture. Delpey (1941: 20-21) recog-
nized three subgenera within Campanile:
Diozoptyxis Cossmann, 1896, Campanilopa
Iredale, 1917 and Campanile Fischer, 1884,
s.s. She noted that Campanile gomphoceras
Bayan, 1870, of the Eocene, lacked a columel-
lar plait and closely resembled Campanile
gigas (Martin) of the Piocene of Java which
she considered to be the direct ancestor of the
Recent Campanile symbolicum. Delpey
(1941) suggested that the genus migrated
from the Tethys Sea to Australia and that
Campanile symbolicum (cited as Cerithium
laeve) was the modern survivor of a long line-
age within the family Campanilidae. She con-
sidered the earliest representatives of the
group to have arisen from the Nerineidae, a
fossil group characterized by elaborate
parietal, palatal and columellar folds, and
noted the resemblance of some species in the
subgenus Diozoptyxis to the nerineids.
Diozoptyxis is not regarded as a nerineid
(Sohl, personal communication). Although | do
not agree with her about relationships with the
nerineids (see Discussion, this paper), her
arguments regarding Campanile phylogeny
appear to be both comprehensive and reason-
able. While | do not consider it within my ex-
pertise to comment on these speculative rela-
tionships, | concur with her conservative clas-
sification of the family Campanilidae. In this
paper | will deal only with Campanile symboli-
cum, and exclude taxonomic treatment of the
fossil species and supraspecific taxa. The
question of the generic allocations of the
numerous fossil species in relation to the
Recent one are beyond the scope of this
paper.

Campanile symbolicum Iredale
(Figs. 1-9)

Cerithium leve Quoy & Gaimard, 1834: 106-
108; 1833, Atlas, pl. 54, figs. 1-3, non-

binomial (holotype: ММНМР, not registered;
type-locality: Port of King George, Australia
(= King George Sound, Western Australia)
[non С. laevis Perry, 1810].

Cerithium truncatum Gray [in] Griffith &
Pidgeon, 1834: pl. 13, fig. 1 (error, cor-
rected in Index to С. laeve Gray; see Ire-
dale, 1917: 326).

Cerith. leve Quoy [sic], Kiener, 1841: 14-15,
pl. 17, fig. 4.

Cerithium laeve Quoy [sic] Deshayes, 1843:
306-307; Sowerby, 1855: 855, pl. 85, fig.
270; Tryon, 1887: 149, pl. 29, fig. 71;
Cossmann, 1906: 72-73; Thiele, 1931:
215:

Telescopium laeve (Quoy & Gaimard).
Reeve, 1865: pl. 1, figs. 2a, b.

Cerithium (Pyrazus) laeve Quoy [sic]. Kobelt,
1898: 46—47, pl. 10, fig. 1.

Campanile symbolicum lredale, 1917: 326
(new name); Iredale, 1949: 20; Allan, 1950:
88, pl. 17, fig. 24; Wilson & Gillett, 1971: 32,
pl. 12, fig. 1; 1979: 58, pl. 10, fig. 1.

Ceratoptilus laevis (Quoy & Gaimard).
Bouvier, 1887a: 37-38; 1887b: 146, pl. 8,
fig. 33, pl. 9, fig. 38.

Remarks.—The original species name
proposed by Quoy & Gaimard (1834) was
spelled “leve” but most subsequent authors
have used “laeve.” This name is preoccupied
by Cerithium laevis Perry, 1810, which al-
though slightly different in spelling, does not
vary enough to constitute a significant differ-
ence (see Code, Article 58), Quoy &
Gaimard’s name thus becomes a junior pri-
mary homonym. In the original description,
Quoy & Gaimard (1834: 108) remarked that
several hundred individuals were collected in
shallow water and that their shells were
somewhat similar to those of Telescopium,
but were longer and had sharper spires. They
described the external anatomy of the ani-
mals and briefly discussed the internal organs
of the mantle cavity. Some notes on the habi-
tat and sexual state of the specimens were
presented and the shell, animal and opercul-
um are accurately depicted on pl. 54, figs. 1-
3, of the Atlas (Quoy & Gaimard, 1833). Al-
though the Atlas appeared a year earlier than
the description, no Latin name was given;
consequently the Atlas is non-bionomial.

Iredale (1917: 326) noted that the name
Cerithium leve was preoccupied and pro-
posed a new name Campanile symbolicum,
to replace it. Iredale (1917: 326) also pointed
out that the name Cerithium truncatum Gray,
1834, was an error. Griffith & Pidgeon (1834)

CAMPANILE ANATOMY AND SYSTEMATICS 283

figured the shell under the name truncatum,
but this was a careless slip and was corrected
in the index of the same work.

DISCUSSION

Campanile symbolicum is a relict species
representing the end of a long lineage of large
mesogastropods in the family Campanilidae.
The anatomical evidence derived from the liv-
ing species places this group within the super-
family Cerithiacea. | agree with Delpey (1941)
that this large family probably comprised sev-
eral genera that underwent a widespread
adaptive radiation in the Tertiary. The family is
well represented by many fossil species that
were abundant in the Tethys Sea and is rep-
resented in New World deposits by the en-
demic genus Dirocerithium Woodring &
Stenzel, 1959. Woodring (1959) pointed out
the Tethyan affinities and also noted the close
resemblance of Campanile gomphoceras
Bayan, 1870, of the European Eocene, to
Dirocerithium. He also regarded Bellatara
Strand to be closely related to this lineage. In
the Old World the family comprised numerous
species in the genera Diozoptyxis Cossmann,
1896, Campanilopa Iredale, 1917 and
Campanile Fischer, 1884. It is apparent that
the entire fossil assemblage is in need of fur-
ther revision and study before the composi-
tion and lineages within the family can be
understood, a task beyond the scope of this
paper.

| do not believe that sculptural differences
such as placement and number of columellar
plaits, between the living species and the fos-
sil taxa warrant a separation of the Recent
species from the fossil groups. While the liv-
ing species may not be congeneric with some
of the fossils, it is surely in the same family. It
is apparent that the family comprises several
зирга-зресйс categories that differ from the
living species and future taxonomic studies of
the family may show the need for a new
genus to accommodate the Recent form. In
this paper | prefer to be conservative and refer
the living species to the genus Campanile.

The shell of the living species does not dif-
fer substantially from that of the fossils (see
Delpey, 1941) and present understanding of
plate tectonics provides sufficient explanation
for the linkage between the Tethyan fossils
and the living species in southwest Australia
without having to invoke any farfetched migra-
tion theories.

The pitted surface of Eocene Campanile

fossils noted by Wrigley (1940: 111) resem-
bles the pattern seen on the thick, calcified
periostracum or “intritacalx” of the living spe-
cies. | suggest that the pits on the fossils are
periostracal in origin and that this is probably
a family character.

Delpey (1941) noted that some of the fossil
campanilids with elaborate parietal, palatal
and columellar folds closely resembled mem-
bers of the Nerineidae and suggested that the
Campanilidae arose from the nerineid line-
age. This is most unlikely because nerineids
have heterostrophic protoconchs and deep
anal sulci and are considered to be in the
subclass Euthyneura (Taylor & Sohl, 1962:
11, 16-17). Thus, any resemblance between
these two groups is due to convergence and
does not imply relationship.

Both the living species and the fossil taxa
have been referred to genera within the family
Potamididae Fleming by Sowerby (1865) and
Iredale (1917: 1949) but | do not concur. The
ecology and anatomy of Campanile differ
substantially from those of the amphibious
potamidids which have multispiral, circular
opercula, differently arranged open pallial
gonoducts, thin, ridge-like osphradia and long
snouts with radulae that frequently bear basal
cusps.

The elongate, multi-whorled shell, the aper-
tural physiognomy, corneous operculum,
taenioglossate radula, aphallic males and
open pallial gonoducts in both sexes are con-
servative characters found in nearly all
cerithiaceans; however, the combined ana-
tomical features of sensory, reproductive,
alimentary and nervous systems of Campanile
are, as far as is known, unique among the
Cerithiacea and support its allocation to a
separate family, the Campanilidae. A discus-
sion of these unique anatomical features and
speculation about the phylogenetic relation-
ship of Campanile to other higher cerithi-
acean taxa follows.

The external anatomy of Campanile differs
from that of other cerithiaceans in several fea-
tures: Campanile has a deep ciliated pedal
gland around the edge of the entire sole of the
foot (Fig. 48, cf) whereas in cerithiids and
some potamidids there is only a propodial fur-
row. In a few potamidids there is a centrally
placed pedal gland. The entire mantle edge of
Campanile has papillae on it, although these
are reduced ventrally (Fig. 34-B, mp), while in
the cerithiids the ventral part of the mantle
edge is always smooth. In vermetids and
pleurocerids, the entire mantle edge is
smooth and in the turritellids completely

284 HOUBRICK

papillate; while in the thiarids the condition is
mixed, depending upon the genus or species.
The short, thick snout of Campanile, noted by
Bouvier (1887b), differs from that of most
other cerithiids which have longer and more
extensible snouts.

The columellar muscle of Campanile is un-
usual among cerithiaceans in that it is unusu-
ally long and forms a long prominence at its
proximal end (Fig. ЗА-В, cm). This may en-
able the animal to withdraw more deeply into
its shell. A similar columellar muscle has been
depicted by Morton (1965) and Hughes
(1978) for the members of vermetid genera
Vermetus, Serpulorbis, Dendropoma and
Petaloconchus, all capable of deep with-
drawal into their shells.

The short, oval, bipectinate osphradium
(Fig. 4A, os) differs from those of all other
known cerithiaceans and most mesogastro-
pods where the osphradium is normally a long
slender structure that traverses the length of
the mantle cavity adjacent to the ctenidium.
Other mesogastropods with a short bi-
pectinate osphradium include members of the
Cypraeacea, Calyptraeidae, and the genera
Velutina and Balcis. In Campanile, the
osphradium is unusual in that it is placed
anteriorly in the mantle cavity, and both its
placement and anatomy are identical to those
seen in most neogastropods.

The extension of the hypobranchial gland
and its modification by folding into tiny leaflets
adjacent to the anus (Fig. 4A, /hg) are ana-
tomical features unrecorded for other
cerithiaceans. The presence of numerous
elongate goblet cells in this tissue testifies to
its secretory ability. lt may produce additional
mucus to bind fecal pellets as they pass out
the exhalant siphon and down the ciliated
groove on the right side of the foot.

The pallial oviduct of Campanile is simple in
comparison to those of the cerithiids,
modulids, turritellids and vermetids in that the
laminae comprising it lack the internal tubes
and bursae associated with spermatophore
retention and sperm transfer. Instead, the pal-
lial oviduct is a simple slit tube (Fig. 4C), but
one in which the transverse interior folds of
the distal end of the laminae are elaborated
into rounded filaments forming a large albu-
men gland (Fig. 4A, ag) unlike anything seen
so far in other cerithiaceans. As seen earlier,
the spawn mass produced by the animal is
quite large and gelatinous (Fig. 8A-B) and it is
possible that this gland and the mid-glandular
part of the oviduct contribute to its formation.

One of the more unusual features of
Campanile reproductive anatomy is the pres-
ence of a sac-like seminal receptacle that
bulges into the pericardial sac (Fig. 4А-В, sr,
ps). | know of nothing else like this in any
cerithiacean, although several rissoacean
species store sperm in the pericardium
(Ponder, personal communication). The ar-
rangement is rare among prosobranchs.
There is convincing anatomical evidence to
suggest that Campanile is a protandric
hermaphrodite. A seminal receptacle is pres-
ent at the proximal left side of the pallial
gonoduct in both sexes but is more fully de-
veloped in females where it may consist of
several lobes. It appears that larger individu-
als are females and smaller ones males. Sec-
tions of the gonads of larger snails revealed
only developing ova while those of smaller
animals clearly showed seminiferous tubules
filed with varying stages of developing
spermatozoans. Although | found no histo-
logical evidence of simultaneous hermaphro-
ditism, transitional stages between sexes
should be looked for by future workers.

Sections of the seminal receptacle (Fig. 7A,
D) show that the branching chambers con-
taining oriented sperm have relatively smooth
walls (Fig. 7A, lower chambers; Fig. 7D, C,
sp), while the empty chambers are villous and
ciliated (Fig. 7A, upper chambers; C, ctb). The
receptacle thus appears to be divided into two
kinds of interconnected branching chambers.
The empty tubes and chambers may assist in
sperm transport, but their exact function re-
mains undetermined.

Another unusual aspect of Campanile re-
productive biology is the bright pink color of
the head-foot in ripe animals, particularly
females. | know of no other cerithiacean in
which this phenomenon has been recorded
and its significance is unknown.

The presence of what appeared to be a dis-
integrating spermatophore in the pallial ovi-
duct needs reconfirmation; however, most
cerithiaceans such as the cerithiids, modulids
and vermetids produce spermatophores. If
Campanile has only eupyrene sperm, it is
unusual because all cerithiaceans heretofore
studied show spermic dimorphism.

The spawn of Campanile (Fig. 8A-B) are
unusual because of their large size, high
gelatinous content, the lack of individual
hyaline capsules for each egg and the pres-
ence of a chalaza connecting the egg cap-
sules. The spawn resemble those of opistho-
branchs and polychaetes more than those of

CAMPANILE ANATOMY AND SYSTEMATICS 285

prosobranch spawn. Robertson (1976: 231)
pointed out that chalazae are characteristic of
opisthobranchs and primitive pulmonates, but
among the prosobranchs are known only in
the genus Valvata and in members of the
Architectonicidae, which are not typical of the
group. The connections between egg cham-
bers in Campanile may not be truly homolo-
gous with the chalazae of opisthobranch
spawn. The presence of eggs within mucous
capsules rather than hyaline capsules is also
unusual and the fact that several eggs may be
in an individual capsule points to the possibil-
ity of nurse eggs. While the high number of
eggs per spawn mass and moderate size of
individual eggs would seem to indicate indi-
rect development, the developmental mode
appears to be direct or demersal. Evidence
for non-pelagic development is strong: ad-
vanced veliger stages with tiny velar lobes
were observed in preserved spawn and the
embryonic shell (Fig. 2a-c) is smooth, bul-
bous, lacks a sinusigera notch and has only
one and a half whorls.

All of the above observations raise more
questions and it is obvious that more careful
work on the developmental biology of
Campanile is needed. A

While most cerithiid jaws are thin and con-
sist of many tiny, flat plates, those of
Campanile (Fig. 2d-e, hy) are very thick and
structurally complex, as outlined previously.
The significance of this difference is unclear,
but their structure is undoubtedly related to
their ontogeny and needs further detailed
study. The typically taenioglossate radula
(Fig. 6A-D) is short in comparison to the size
of the animal and has fewer rows of teeth than
the radulae of other cerithiids which are much
smaller animals than Campanile. This is pe-
culiar because most snails that graze on
coarse substrates, as does Campanile, have
long radular ribbons. The radula of Campanile,
however, is wide and robust and cusps of the
anterior rows of teeth are only slightly worn.

The thin septum behind the nerve ring that
divides the cephalic hemocoel of Campanile
is more anterior than the transverse septum of
trochids which lies where the mid-esophagus
joins the posterior esophagus (Fretter, in litt.).

The paired salivary glands and their ducts
lie anterior to the nerve ring (Fig. 5A), as in the
cerithiids, modulids (Houbrick, 1980),
vermetids (Morton, 1951: 29) and in nearly all
rissoids (Davis et al., 1976: 276; Ponder,
personal communication). This is further
documentation that the location of salivary

glands and their ducts is a variable feature
among the mesogastropods.

The presence of paired buccal pouches
(Fig. 5A, bp) in Campanile is noteworthy,
because they are unknown among other
cerithiaceans. | previously thought that the
Salivary glands of Cerithium were buccal
pouches and stated that their ducts passed
through the nerve ring, but this was erroneous
(Houbrick, 1974: 43). Although found in
littorinids, it appears that the cerithiids,
modulids, vermetids and turritellids all lack
buccal pouches. It is interesting to note that
buccal pouches and anterior salivary glands
are required for neogastropod ancestors.

The mid-esophagus loses all traces of the
dorsal and ventral food channels but is un-
usual in having shallow lateral folds (Fig. 7E).
Campanile differs from anatomically known
cerithiids and modulids in lacking an esoph-
ageal gland, but the vermetids and turritellids
known also lack this gland. Although it is not
uncommon for gastropods to have loose con-
nective tissue surrounding the esophagus,
the mass of loose connective tissue that sur-
rounds the mid-esophagus of Campanile (Fig.
7E, cnt) is unusually large and noteworthy.
Although this tissue superficially looks like an
esophageal gland, sections show that it has
no glandular elements or connections with the
esophagus. A further distinction of this region
is the thin muscular sheet in the middle of the
connective tissue surrounding the тю-
esophagus (Fig. 7E, ml). The function of this
loose connective tissue and its thin muscular
sheet was not determined.

The stomach of Campanile has a well-
developed style sac (Fig. 5B, ss), but a cuticu-
lar gastric shield is lacking, and | was unable
to find any trace of a style, even in freshly
collected animals. It is possible that a style is
present only at certain times, as in some bi-
valves. One of the most unusual features of
the stomach is the series of leaflets spirally
arranged in a deep pit located in the sorting
area (Fig. 5B, s/). Although | have seen a
similar structure in the stomach of Gourmya
gourmyi (Crosse), which is a cerithiid snail, |
know of no structure like this in any other
prosobranchs with the exception of the volute
Alcithoe, for which Ponder (1970: 19) de-
scribed similar gastric leaflets. In Alcithoe,
they are arranged in parallel rows rather than
in a Spiral pit, but the structure and ciliary cur-
rents of each leaflet are the same. Ponder
noted that they are an efficient sorting device
in a relatively uncomplicated stomach; this is

286 HOUBRICK

in direct contrast to the complex stomach of
Campanile. The pit and leaflets probably deal
with the larger particles and this is a modifica-
tion from other cerithiaceans. The posterior of
the stomach, which | interpret as the vestige
of a spiral caecum, is another distinctive
structure (Fig. 5B, sc). Reduced spiral caeca
have been recorded in other mesogastro-
pods, such as some turritellids, cerithiids and
calyptraeids, by Fretter & Graham (1962: 224)
but in Campanile this structure is much larger
and more conspicuous.

A mixture of loose and condensed neural
elements including dialyneury and zygoneury
exists in Campanile. It is difficult to assess the
significance of this arrangement of the nerv-
ous system because not enough is known of
other cerithiacean nervous systems to make
meaningful comparisons with Campanile.

As seen т the foregoing discussion,
Campanile falls well within the cerithiacean
anatomical groundplan but the relationship of
the Campanilidae to other cerithiacean fami-
lies is more difficult to assess. It appears to be
closest to the Potamididae and Cerithiidae in
general physiognomy and ecology, but is
probably related to them only distantly. There
are several anatomical features of Campanile
that are reminiscent of neogastropods.
Among these are the short, distally located
bipectinate osphradium, anterior position of
Salivary glands and ducts relative to the nerve
ring, and the complex spirally arranged leaf-
lets in the sorting area of the stomach al-
though the latter are not typical of neogastro-
pods. The presence of a calcified periostra-
cum or intritacalx is known in some rissoids
and epitoniids but is not common in meso-
gastropods. Although | do not believe that
these features indicate a relationship between
Campanile and the neogastropods, they are
unusual and set this group apart from other
cerithiaceans and most mesogastropods.

The Campanilidae is an old family as are
other cerithiacean marine families such as
the Cerithiidae, Potamididae, Vermetidae,
Turritellidae, Dialidae, Cerithiopsidae, and
the Modulidae. All these families were present
in the late Cretaceous and appear to have
undergone little change in basic shell form
since then. The cerithiaceans appear to con-
stitute a large monophyletic assemblage. All
share the basic primitive anatomical traits of
open pallial gonoducts and aphallic males
and are algal-detrital feeders with taenio-
glossate radulae and complex stomachs.

Nearly all members of the group have a crys-
talline style.

In general, each cerithiacean family has
radiated into a distinctive spatial, trophic
niche. It is obvious that the success of many
families is due to basic morphological innova-
tions in shell and soft parts or to physiological
modifications that led to new adaptations in
feeding and exploitation of new habitats such
as the estuarine and fresh-water biotopes.
Other modifications have occurred in the re-
productive systems (spermatophores,
spermatozeugma, dimorphic sperm, complex
ducts in open pallial gonoducts, brooding
chambers), but the adaptive significance of
these modifications is not always clear. A brief
summary of the major cerithiacean families
and their ecological niches follows.

The Turritellidae, characterized by long
coiled shells, is an abundant subtidal group of
animals that tend to live on soft substrata
where they are detrital-filter feeders (Graham,
1938; Fretter & Graham, 1962). The Vermet-
idae is an intertidal to subtidal, sessile group of
snails with uncoiled shells usually found on
hard substrata feeding on detritus by ciliary
mechanisms and mucous nets (Morton, 1965;
Hadfield, 1970; Hadfield et al., 1971; Hughes,
1978). The Potamididae comprise a large
group of intertidal estuarine amphibious snails
with turreted shells that are grazers on algae
and detritus. They are frequently large animals
and are common in tropical mangrove habi-
tats, salt marshes and muddy environments.
The Cerithiidae are a large, complex family of
intertidal to subtidal snails with turreted shells
common in tropical areas. This group is pri-
marily composed of algal-detritus feeders and
has radiated into a variety of habitats including
coral reefs, rocky beaches, sandy lagoons,
mud flats and grass beds (Houbrick, 1974;
1978). The Pleuroceridae, regarded as the
freshwater branch of the Cerithiidae, com-
prises a large family of turreted snails that live
in well-oxygenated water in temperate and
tropical regions (Morrison, 1954). The
Dialidae, Litiopidae, and Diastomidae are little
known families, the former comprising small
snails common in tropical areas and the latter a
largely extinct group of larger snails with tur-
reted shells and with only one living species.
The Modulidae is a small family of subtidal
snails with trochoid shells that live in grass
beds or on coral reefs (Houbrick, 1980). The
Planaxidae is a small group of tropical snails
that live in the rocky intertidal and brood their

CAMPANILE ANATOMY AND SYSTEMATICS 287

young in special incubation chambers in the
head (Ponder, 1979). The Thiaridae, a large
family of freshwater snails, tend to be parthe-
nogenetic and ovoviviparous and are thought
to be derived from the marine Planaxidae
(Morrison, 1954). The Cerithiopsidae are small
multispired snails that have an acrembolic
proboscis (Fretter, 1951) and feed on
sponges. They are no longer considered
cerithiaceans (Fretter, 1979).

The major adaptive radiations of cerithi-
acean marine families occurred at the end of
the Cretaceous and it is not at all clear from
the fossil record or from our knowledge of
anatomy how these groups are related to
each other. The Campanilidae stands apart
from the other families in some aspects of
anatomy and is also noteworthy because of
the large size attained by many of its mem-
bers. Although it is not uncommon for some
species of other cerithiacean families such as
the Turritellidae, Vermetidae, Potamididae
and Cerithiidae, to be large animals, the
Campanilidae developed this trait to an extra-
ordinary degree.

These large snails were most common in
the early Tertiary when they seem to have
reached an evolutionary peak in number of
species. Members of the Campanilidae prob-
ably played the same ecological role т
Tethyan shallow water ecosystems as Recent
Strombidae in similar contemporary habitats.
They undoubtedly were feeders on epiphytic
algae and occupied the same trophic niche as
do large snails of the living strombid genera
Strombus, Lambis and Tibia.

The Strombidae became established in the
late Eocene to early Miocene and flourished
during the Pliocene and early Pleistocene
(Abbott, 1960: 33). Competition with this
trophically similar group of large snails prob-
ably led to the diminution in species of the
Campanilidae. The living survivor, Campanile
symbolicum, is now confined to southwest
Australia where only one small stromb spe-
cies occurs, Strombus mutabilis Swainson
(Abbott, 1960: 74). It is noteworthy that south-
ern Australia harbors several other Tethyan
relicts, the monotypic gastropod Neodia-
stoma melanoides (Reeve), family Diastom-
idae, and the bivalve Neotrigonia, family
Trigoniidae, although the latter lives all
around Australia.

The actual reasons for the virtual extinction
of the Campanilidae are unknown, but sea
level changes and fluctuating temperatures

associated with the closure of the Tethys Sea
undoubtedly placed additional stress on this
group of remarkably large gastropods.

ACKNOWLEDGMENTS

| am indebted to Dr. Fred Wells of the West-
ern Australian Museum, Perth, for his kind as-
sistance and for the use of laboratory space
and a vehicle for field work during my stay
there. | also thank Ms. Miriam Rogers for her
help in collecting specimens and for process-
ing field material.

For examination of specimens in their
charge | thank Dr. George Davis, Academy of
Natural Sciences of Philadelphia, Dr. William
K. Emerson, American Museum of Natural
History, Dr. Brian Smith, National Museum of
Victoria, and Dr. Winston Ponder, The Aus-
tralian Museum, Sydney.

| thank Dr. Robert Black of the University of
Western Australia for sending me preserved
samples of spawn and for information about
spawning.

Histology was done at the Smithsonian In-
stitution’s Fort Pierce Laboratory. | thank Dr.
Mary Rice for her kind assistance in using this
facility, and Mrs. June Jones for typing the
Original draft of this paper. The scanning
electron micrographs were supplied by the
Smithsonian Scanning Electron Microscope
Lab. All other photography was done by Mr.
Victor Krantz of the Smithsonian Photo-
graphic Services.

This research was accomplished with the
aid of a Smithsonian Research Award.

| thank Dr. Winston Ponder and Dr. Vera
Fretter for critically reading the first draft of
this paper.

LITERATURE CITED

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ANDRUSOV, D., 1953, Nove Paleontologicke
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BOUSSAC, J., 1912, Essai sur l'évolution des
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288 HOUBRICK

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MALACOLOGIA, 1981, 21(1-2): 291-336

THE GALAPAGOS RIFT LIMPET NEOMPHALUS: RELEVANCE TO
UNDERSTANDING THE EVOLUTION OF A MAJOR
PALEOZOIC-MESOZOIC RADIATION!

James H. McLean

Los Angeles County Museum of Natural History, Los Angeles, California 90007, U.S.A.

ABSTRACT

Neomphalus fretterae, new species, genus, family, and superfamily, was first collected in
1977 at the vents of thermal springs along the Galapagos deep-sea spreading center at depths
of 2,478 to 2,518 m. Shells reach 30 mm in diameter and are cap-shaped with a horizontally
lying initial coiled phase. The shell is protected by periostracum and is composed of lamellar
aragonite. In form and function Neomphalus is convergent with the Calyptraeidae, having a
flattened neck and a deep mantle cavity on the left with long gill filaments extending to the food
groove on the right. Neomphalus is the first known gastropod with a bipectinate gill modified for
filter feeding.

As further detailed in the adjoining paper on internal anatomy (Fretter, Graham & McLean,
1981), Neomphalus has such archaeogastropod characters as a rhipidoglossate radula, bi-
pectinate ctenidium, epipodial tentacles, and anterior loop of the intestine. Features of the
mesogastropod level of organization include loss of the right pallial complex, a monotocardian
circulatory system, expanded left kidney, and glandular gonoducts. Unique features are: 1) a
dorsal food groove, which leads to the mouth over the right cephalic tentacle rather than under it
as in all other filter-feeding gastropods, 2) a mantle cavity not enveloped by the shell muscle on the
left side, 3) posteriorly directed cephalic tentacles, 4) reproductive specializations: the male
with the left tentacle enlarged to form a copulatory organ, and the female with a separate seminal
receptacle.

The first postprotoconch whorl is coiled; growth stoppage in the second postprotoconch whorl
on the columellar lip prevents the muscle from enveloping the mantle cavity on the left, but forces
lip expansion on the right to produce the limpet shell form.

There are no living relatives, nor has any fossil record of Neomphalus been found, yet the
ctenidium is so adaptive that a radiation on this theme must have taken place, and the highly
specialized Neomphalus can only represent one ultimate expression of this basic plan. Paleon-
tologists have recently hypothesized that the extinct Euomphalacea, which underwent a major
radiation in the Paleozoic and declined in the Mesozoic, were filter feeders because their dis-
coidal or open coiled shells with radial apertures differ from those of motile gastropods having
tangential apertures and the capacity to balance the shell over the cephalopedal mass. The
anatomy of Neomphalus could function in a coiled shell and would explain the euomphalacean
anatomy, the differences between Neomphalus and euomphalaceans being about equivalent to
differences betwen calyptraeids and turritellids. As in turritellids the operculum of euomphala-
ceans would loosely block the aperture in feeding position. The columellar muscle in the
euomphalaceans would be at the right of the cephalopedal mass, instead of ventral to it as in
those motile gastropods that balance the shell over the cephalopedal mass. The coiling axis in
euomphalaceans has to shift relative to the substrate from horizontal to vertical during growth, as
shell-balancing capacity is lost and filter feeding replaces grazing. Because the position of the
columellar muscle in Neomphalus is to the right of the cephalopedal mass and because
Neomphalus also shifts the coiling axis of its initial whorls, Neomphalus is the logical limpet
derivative of an euomphalacean.

The discoidal euomphalaceans became extinct in the Cretaceous, having no defense against
shell-crushing predators that arose in the Mesozoic, but the limpet derivative is protected against
such predators and exploits the abundant chemosynthetic bacterial food source not accessible
to soft-substrate-dwelling animals. During the Mesozoic, hydrothermal vents may have been
accessible along rift zones in shallow water, providing stepping stones to deep-water rift sys-
tems. The rift-vents in deep water fortuitously lack such usual molluscan predators as drill snails

1Contribution number 17 of the Galapagos Rift Biology Expedition, supported by the [United States] National Science
Foundation.

(291)

292

McLEAN

and sea stars; thus, the rift-vent habitat has been a stable refugium for a relict family at least
since the Cretaceous, the period of the last surviving euomphalaceans.

Only the Pleurotomariidae share with the Neomphalidae the absence of afferent support to the
ctenidium. The Euomphalacea can be independently derived from the Pleurotomariacea, upon
loss of the right pallial complex, probably from an early pleurotomariacean stock of flat-lying
discoidal shells with a slit on the upper whorl surface, as the Ordovician Lesueurilla. The unique
dorsal food groove of Neomphalus is here interpreted as a primitive character. The tips of
filaments from paired ctenidia, modified for filter feeding, could have converged upon a dorsal
food groove in this group of early pleurotomariaceans, the shells of which are no better designed
for locomotion than those of euomphalaceans.

The new archaeogastropod suborder Euomphalina, to include the superfamilies Euom-
phalacea and Neomphalacea, is proposed, an independent line derived from early pleuroto-
mariaceans. It has attained the mesogastropod level of advancement in its circulatory and
reproductive systems but retains the primitive characters of the rhipidoglossate radula and the
bipectinate ctenidium.

Possible affinities of other extinct archaeogastropods are discussed in Appendix 1, with the
conclusion that Macluritacea and Clisospiracea are lineages apart from Euomphalacea and
Trochacea. Pseudophoracea, Platyceratacea, Anomphalacea, Microdomatacea, and Palaeo-
trochacea may have had the pallial complex of the Trochacea.

In Appendix 2 the Liotiidae are recognized in the Paleozoic, making the Trochacea older than
previously supposed, and the Craspedostomatacea and Amberleyacea are merged with the

Trochacea.

INTRODUCTION

Strange new deep-sea communities asso-
ciated with thermal springs along sea-floor
spreading centers have recently been dis-
covered both at the Galapagos Rift (Ballard,
1977; Lonsdale, 1977; Corliss & Ballard,
1977: Corliss et al., 1979; Crane & Ballard,
1980) and the East Pacific Rise (Corliss et al.,
1979; Spiess et al., 1980). Chemosynthetic
bacterial production deep within the springs
provides a source of food (Rau & Hedges,
1979; Karl et al., 1980; Jannasch & Wirsen,
1979, 1981). Another source of food derived
from photosynthetic sources may be made
accessible by advection currents through the
vents (Enright et al., 1981). The hydrothermal
vent communities are richly provided with
filter-feeding animals, predators, and a con-
spicuous gutless animal the vestimentiferan
pogonophoran Яга pachyptila Jones, 1981.
Questions in the fields of ecology, physiology,
reproduction, dispersal, and taxonomic ori-
gins of the rift-vent species have engendered
an extraordinary interest among marine biolo-
gists. Nearly all members of the rift-vent com-
munity are new species.

Mollusks are conspicuous members of
these communities. In addition to two large
bivalve species, a mytilid and the large white
clam, Calyptogena magnifica Boss & Turner,
1980, there are several limpets. The largest of
the limpets from the Galapagos Rift is de-
scribed here as the new genus and species
Neomphalus fretterae. lts anatomy is so un-

like that of any living gastropod that it can not
be assigned to an existing superfamily or
even to a suborder in the Gastropoda.

The external anatomy resembles that of the
mesogastropod family Calyptraeidae, having
a similar flattened neck, a deep mantle cavity
on the left side, and long gill filaments con-
verging upon a food groove. Unlike the
calyptraeids, in which the gill is monopecti-
nate, Neomphalus has a bipectinate gill, with
filaments on both sides of the axis. Bipecti-
nate gills are characteristic of the Archaeo-
gastropoda, the oldest and most primitive
order of prosobranchs. Additional archaeo-
gastropod features include the epipodial
tentacles surrounding the foot and the
rhipidoglossate radula. Unlike such other
single-gilled, rhipidoglossate archaeogastro-
pods as the Trochacea and Neritacea, the
neomphalid heart is monotocardian, having
but a single auricle as in mesogastropods.
Other mesogastropod-like features of
Neomphalus include expansion of the left
kidney to serve as a cavity in which some
organs lie, and reproductive advancements
that include glandular gonoducts, a copula-
tory organ in males and a seminal receptacle
in females. The internal anatomy of
Neomphalus and its affinity to other living
gastropods is treated in a separate paper in
this issue of MALACOLOGIA (Fretter,
Graham & McLean, 1981).

One must assume that Neomphalus repre-
sents an evolutionary line that underwent an
adaptive radiation, as have nearly all animal

GALAPAGOS RIFT LIMPET NEOMPHALUS 293

groups in which a morphological innovation,
in this case the unique filter-feeding ctenidi-
um, has opened a new feeding zone to ex-
ploitation.

The absence of living relatives suggests
that the radiation must have taken place in the
past. Yet, no fossil record of this limpet has
been found. However, because all limpets
derive from coiled predecessors, the search
for relatives may be directed to the extinct
coiled groups. Archaeogastropods were the
dominant gastropods in the Paleozoic, the
period in which the origins of all other higher
categories of living archaeogastropods took
place.

Because the limpet shell form imposes few
constraints upon anatomy, many features of
limpet anatomy are likely common to the
coiled predecessor. There are some groups
of Paleozoic gastropods that seem so poorly
designed for locomotion that they have re-
cently been considered to have been seden-
tary and therefore likely to have been filter
feeders. These groups, the Macluritacea and
the Euomphalacea, are prime candidates as
predecessors to Neomphalus. The discussion
section of this paper presents the case for
Neomphalus as a limpet derivative of the
Euomphalacea. The neomphalid mantle
cavity is suited to function within a coiled
shell. Apart from the ease with which the
neomphalid mantle cavity can account for fil-
ter feeding in euomphalaceans, there are
clues in the shell ontogeny of Neomphalus
that also suggest a derivation from the
Euomphalacea.

The two superfamilies Macluritacea and
Euomphalacea have been united in the sub-
order Macluritina (Cox & Knight, 1960), but
this relationship has recently been questioned
by paleontologists; the differences are suffici-
ently pronounced that subordinal separation
can be justified. As this has not yet been
done, the formal proposal of the suborder
Euomphalina, to include the superfamilies
Euomphalacea and the new superfamily
Neomphalacea, is given at the conclusion to
the discussion section in this paper.

Some other extinct superfamilies of ar-
chaeogastropods were considered as possi-
ble predecessors to Neomphalus. My opin-
ions about feeding modes and affinities of
these groups are given in Appendix 1. Be-
cause the Euomphalacea have shell char-
acters that overlap those of the Trochacea, an
effort has been necessary to define the shell
characters that distinguish the two groups.

Few arguments could be found to preclude
many of the extinct groups from having the
pallial complex of the Trochacea. The evi-
dence seems _ sufficient to merge the
Craspedostomatacea and Amberleyacea with
Trochacea, as discussed in Appendix 2.

MATERIALS AND METHODS

The thermal springs along the spreading
axis of the Galapagos Rift were first observed
from the deep submersible research vessel
ALVIN in February 1977. Although biological
collecting had not been anticipated, pieces of
volcanic rock (Fig. 12A) were retrieved with
the mechanical arm of ALVIN. Limpet speci-
mens ranging in diameter from 7 to 30mm
were removed aboard the support ship and
were transmitted to me in June 1977. These
came from the vent-fields named Oyster Bed
(dives 723 and 726) and Garden of Eden
(dive 733).

Second and third expeditions were made to
the Galapagos Rift site in February and
December 1979 by biologists from Woods
Hole Oceanographic Institution and Scripps
Institution of Oceanography (Ballard &
Grassle, 1979). Small specimens of Neom-
phalus were recovered from samples of the
mytilid collected at the Garden of Eden vent-
field (dive 884) and were transmitted to me.

All specimens were originally fixed in 4%
buffered formalin and were subsequently
transferred to 70% ethyl alcohol. Some speci-
mens were dissected. Transverse and sagittal
sections of males and females were made.
Material for sectioning was embedded in
paraffin; sections were cut at a thickness of
15 um and stained with Mayer's hematoxylin
and eosin. Shells of two small specimens
were examined with a scanning electron mi-
croscope (SEM), and the intact animals of two
others were critical-point dried for SEM ex-
amination. The radula was also examined
with the SEM.

The internal anatomy of Neomphalus, its
bearing on feeding and reproduction and the
relationship to other living gastropods is
treated separately by Fretter, Graham &
McLean in this issue of MALACOLOGIA. The
discussion section in the present paper there-
fore follows the discussion in the joint paper.

A report on the shell structure by Roger L.
Batten, American Museum of Natural History,
is in preparation and will be published sepa-
rately.

294 McLEAN

In this paper frequent references are made
to extinct genera and families of archaeo-
gastropods. All are diagnosed and illustrated
in the archaeogastropod volume of the
Treatise on Invertebrate Paleontology (1960),
in which the Paleozoic groups were treated by
J. B. Knight, R. L. Batten & E. L. Yochelson,
those of the Mesozoic by L. R. Cox, and those
of the Cenozoic by А. М. Keen and В. Robert-
son. Knight’s (1941) “Paleozoic Gastropod
Genotypes” provides photographic illustra-
tions useful for comparison with the shell
drawings in the Treatise. Authors, dates, and
type-species of genera are not given here;
citations are readily available in these works.

SYSTEMATICS AND DESCRIPTIONS
NEOMPHALACEA McLean, new superfamily

Diagnosis: Having the characters of the
family as follows:

NEOMPHALIDAE McLean, new family

Diagnosis: Shell cap-shaped, composed of
lamellar aragonite and having an adherent
periostracum; protoconch and first postproto-
conch whorl with coiling axis perpendicular to
final aperture; first whorl rounded, suture
deep; conversion to limpet form in second
postprotoconch whorl by process of lip ex-
pansion on upper half of whorl and growth
stoppage on columella; radula rhipido-
glossate; foot with anterior mucous gland and
epipodial tentacles bunched along posterior
sides of foot; shell muscle crescent-shaped,
enveloping the visceral cavity but not the
mantle cavity or pericardial cavity; mantle
cavity deep, extending entire length of animal
on left side; heart monotocardian, ventricle
not traversed by rectum; right ctenidium and
auricle lacking but represented by prominent
efferent pallial vein in mantle skirt; left ctenidi-
um lacking afferent membrane, attached to
floor of mantle cavity by thickened efferent
membrane; elongate gill filaments arching
over flattened neck to food groove, which cuts
over top of head directly to mouth; left kidney
enlarged to form body cavity; gonads dis-
charging through glandular gonoducts; left
cephalic tentacle of male enlarged to serve as
copulatory organ; seminal receptacle in fe-
male unconnected to genital duct.

Neomphalus McLean, new genus

Diagnosis: With the characters of the family
plus shell features that include a nearly cen-
tral position of the apical whorls, sculpture of
fine radial ribs, and an internal shell ridge
within the area of the muscle scar that in-
creases the area for muscle insertion.

Type-species: Neomphalus fretterae, new
species. Other species are yet unknown but
may be expected at other rift-vent sites.

Etymology: The generic name combines
the Greek prefix neo (new), and the generic
name Euomphalus J. Sowerby, 1814, in
keeping with my theory that the Neomphali-
dae are limpet derivatives of the Euom-
phalacea. The specific name honors Dr.
Vera Fretter, of the University of Reading, in
recognition of her contributions to our under-
standing of the relationships among proso-
branchs.

Neomphalus fretterae McLean, new species
Figs. 1-12

Material: 115 specimens in the initial series,
69 © and 46 G from 3 dives of the ALVIN at
the Oyster Bed and Garden of Eden vent-
fields on the Galapagos Rift: Dive 723, Oyster
Bed, 27 February 1977, 0°47.5'N, 86°08.0'W,
2478-2490 т, 15 $, 5 d; Dive 726, Oyster
Bed, 9 March 1977, same coordinates and
depths, 17 ©, 18 <; Dive 733, Garden of
Eden, 16 March 1977, 0°47.69'N,
86°07.74'W, 2482-2518 m, 37 9, 23 4. Posi-
tion of Oyster Bed from the 1977 expedition,
that of Garden of Eden from the 1979 expedi-
tions; depths from ranges recorded on the
1979 expeditions, courtesy Fred Grassle.

Type Material: The holotype (Figs. 3A, B),
an intact 2 attached to the shell, from dive
723, Oyster Bed, is deposited in the U.S. Na-
tional Museum of Natural History, Washington
(USNM), no. 784637. Designated paratypes
from dives 723, 726, and 733, as follows:
USNM no. 784638, 3 ©, 2 d; Los Angeles
County Museum of Natural History (LACM),
по. 1966, 17 ©, 83, including specimens il-
lustrated in Figs. 1, 4-9, some specimens dis-
sected, 5 specimens sectioned; Museum of
Comparative Zoology, Harvard University,
Cambridge (MCZ), по. 280321, 5 $, 5 6.
Additional paratype lots preserved with the
body attached to the shell, have been sent to
the mollusk departments of the following mu-
seums, the lot consisting of either two $ and
one < or one $ and one $, each specimen

GALAPAGOS RIFT LIMPET NEOMPHALUS 295

individually labeled by sex and dive number:
Academy of Natural Sciences, Philadelphia;
American Museum of Natural History, New
York; Field Museum of Natural History, Chi-
cago; California Academy of Sciences, San
Francisco; Department of Paleontology, Uni-
versity of California, Berkeley; Scripps Institu-
tion of Oceanograpy, La Jolla; National Mu-
seum of Canada, Ottawa; Museo Nacional de
Historia Natural, Santiago; British Museum
(Natural History), London; National Museum
of Wales, Cardiff; Royal Scottish Museum,
Edinburgh; Museum National d'Histoire
Naturelle, Paris; Zoological Museum, Copen-

hagen; Zoological Museum, Amsterdam;
Rijksmuseum van Natuurlijke Historie,
Leiden; Forschungs-Institut Senckenberg,

Frankfurt; Zoological Institute, Academy of
Sciences, Leningrad; P. P. Shirshov Institute
of Oceanology, Moscow; National Science
Museum, Tokyo; Australian Museum, Syd-
ney; National Museum of Victoria, Melbourne;
Western Australian Museum, Perth; National
Museum of New Zealand, Wellington;
Auckland Institute and Museum, Auckland.
Additional Material: USNM 784639, dive
733, 23 specimens, 12 2 and 11 d, associat-
ed with the vestimentiferan Riftia, frozen and
thawed in Bouin’s fixative (which destroyed
the shells) by M. Jones; MCZ 280323, 9 speci-
mens, 1977 expedition, dive number not re-

corded; LACM 67728, Dive 884, Garden of
Eden, 25 January 1979, 17 small specimens
removed from shells and residue associated
with the mytilid bivalve, including specimens
illustrated in Fig. 10. Specimens from dives
723, 726, and 733 not designated as para-
types have been sent to Dr. Vera Fretter, Dr.
Roger L. Batten, and Dr. Richard A. Lutz.

Geographic Range: Oyster Bed, Garden of
Eden, Rose Garden, and Mussel Bed vent-
fields at the Galapagos Rift. Although speci-
mens from the latter two vent-fields have not
been examined, Neomphalus has been iden-
tified by Dr. Fred Grassle and Ms. Linda
Morse-Porteous in the collections from these
vent fields that were made on the January-
February, 1979, expedition.

Description

Shell (Figs. 1, 3, 9, 10): Maximum diameter
of females 30.0 mm, of males 25.5 mm. The
initial series had 30 females 22 mm in diam-
eter or larger but only 3 males that size or
larger. Shell height 0.23 to 0.33 times diam-
eter. Dimensions of holotype: Maximum di-
ameter 30.0, lesser diameter 26.7, height
7.8 тт.

The shell is white under a light-brown
periostracum, moderately elevated and ir-
regular in outline. The adult shell is composed

FIG. 1. Neomphalus fretterae McLean. Shell of mature female, dive 733, Garden of Eden, maximum
diameter 26.6 mm, maximum height 6.5 mm. A) Lateral view from left side, showing the irregular shell
margin. B) Interior view, anterior at top, showing the crescent-shaped muscle scar in the lower left quadrant
and the shell ridge within the anterior arm of the muscle scar.

296 McLEAN

of two layers of lamellar aragonite, an outer
complex crossed-lamellar layer and a thicker
inner radial crossed-lamellar layer.2 The
lamellae of the inner layer are readily visible
under low magnification, running parallel to
lines of growth. The light-brown periostracum
is thin but persistent. It projects beyond the
margin of the shell and has prominent ridges
corresponding to the radial sculpture.

The apex is posterior and slightly to the
right of center, positioned at 0.6 the shell
length from the anterior margin. The proto-
conch (Figs. 10A, B) has 1.2 rounded whorls
and is sculptured with an irregular network of
low ridges. The maximum protoconch diam-
eter is 0.2mm. The first post-protoconch
whorl is rounded and the suture deeply in-
cised; on the second whorl the area next to
the suture has a flattened appearance, and
faint spiral sculpture appears. The growth line
trace on the second whorl continuously in-
creases its extent with growth until it makes a
full circle as the shell diameter reaches
1.8 mm. Further growth takes place along the
entire margin.

The shell is sculptured with radial ribs that
appear at a shell diameter of about 2 mm.
Ribs are well defined, slightly curved until the
shell diameter reaches about 7mm, then
more or less straight. Rib surfaces are round-
ed, with the interspaces about equal to the
width of the ribs. Secondary ribs emerge in
the rib interspaces after the shell attains a di-
ameter of about 7 mm. Every 6th to 10th rib is
stronger than the rest and has a correspond-
ingly strong periostracal ridge. There are 23 to
25 strong ribs on mature shells. Most shells
have irregular concentric interruptions repre-
senting resting stages or growth rings, the first
interruption at a diameter of 6 to 7mm, the
second at a diameter of 9 to 13mm. The
periostracal ridges are stronger after crossing
the first concentric interruption.

The growing edge of the shell is very thin
and fragile and extends in short digitations
corresponding to the rib pattern reflected in
the overhanging periostracum.

The muscle scar (Figs. 1B, 9B) is crescent-
shaped and located entirely within the lower
left quadrant. The scar extends left from the
apical pit and curves to the right, its closest
approach to the shell margin about % the
radius. A shell ridge that is twice as high as
wide originates at the deepest point on the
apical depression. It extends along the inner

2Roger L. Batten, in litt.

border of the muscle scar crescent for a dis-
tance of about Ya the length of the inner mar-
gin of the crescent. The ridge may be 4 mm in
length in large specimens. Its position is en-
tirely within the area of the muscle scar; thus,
it serves to increase the area available for
muscle insertion.

Although thin, the shell of Neomphalus of-
fers highly effective protection. None of the
specimens showed any loss of periostracum
or shell erosion. Specimens remain intact
when dried, although the shell margin and
periostracum may crack.

Similar overhanging periostracum is known
in limpets of the families Capulidae and Hip-
ponicidae. These limpets are immobile—the
overhanging periostracum may function to
provide a tighter seal along the margin.

Shell structure of lamellar aragonite is
known in at least the innermost layer of the
Fissurellidae, Scissurellidae, Skeneidae,
Phasianellidae, Neritidae, Phenacolepadi-
dae, Cocculinidae and the extinct Bellero-
phontacea (Boggild, 1930; MacClintock,
1963, 1967; Batten, 1975; Gainey & Wise,
1980). This is in contrast to the nacreous
aragonitic internal layer of Pleurotomariidae,
Haliotidae, Trochidae, Turbinidae, and
Seguenziidae (Boggild, 1930; Batten, 1972;
Bandel, 1979; Gainey & Wise, 1980), and to
the complex layering in the Patellacea
(MacClintock, 1967).

The protoconch lacks the pointed tip illus-
trated for trochacean species by Bandel
(1975), Rodriguez Babio & Thiriot-Quiévreux
(1975), and Fretter & Graham (1977). The
diameter of the protoconch is well within the
size limits for archaeogastropod protoconchs
tabulated by Bandel (1979).

Radula (Figs. 2A, B,C,D, E): The radula is
rhipidoglossate, with a monocuspidate rachi-
dian, five monocuspidate laterals, and about
20 marginal teeth. The rachidian has a long
main cusp that overhangs half its height, its tip
sharp-pointed and its sides serrate and con-
cave. The base is three times the width of the
overhanging tip and has lateral and basal pro-
trusions that fit in corresponding sockets on
the adjacent lateral teeth. The first lateral has
a basolateral extension and a longer over-
hanging tip than the rachidian. The second
lateral has a longer overhanging tip than the
first lateral and an even broader lateral ex-
tension. Bases of the lateral teeth are notched
to provide space for the overhanging tips of

GALAPAGOS RIFT LIMPET NEOMPHALUS 297

FIG. 2. Neomphalus fretterae. SEM views of radula. A) Full width of ribbon, showing rachidian, 5 laterals,
and sheaths of incompletely separated marginal teeth. x 160. B) Finely fringed tips of marginal teeth. x 1700.
C) Rachidian and first three laterals, showing fine denticulation on both sides of the main cusp of the
rachidian but only on the outer sides of the main cusp of the laterals. x950. D) Rachidian and first three
laterals showing tooth wear. х575. Е) Intact radular ribbon projecting from mouth of preserved specimen.

298 McLEAN

the lateral teeth in the row below. The third
lateral tooth has a narrow overhanging cusp
about as long as that of the first lateral and a
long, curved basal portion with a central
strengthening ridge. The fourth lateral is simi-
lar to the third, and the fifth lateral is thin
throughout and has only a sharp-pointed tip.
The overhanging tips of the maginal teeth
have a large, pointed denticle at the tip, with
as many as 21 smaller comblike denticles on
the sides.

The shafts of the marginal teeth have a
tendency not to separate completely, produc-
ing an irregular arrangement, as has been
noted by Hickman (1980b: 292, fig. 6C), who
suggested that this may be due to a partial
loss of function for these marginal teeth. The
size of the radula is comparable to that of the
Calyptraeidae and not to that of a grazing
archaeogastropod, in which it is about ten
times larger. The shortness of the radular rib-
bon indicates that the teeth are not rapidly
used and replaced. The main function of the
radula must be to rake in the food string, as in
the Calyptraeidae.

The radula of Neomphalus is unlike any
other rhipidoglossate radula. Elongation of
the third, fourth and fifth laterals is unusual,
recalling the elongate teeth in the Pleuro-

tomariidae (Woodward, 1901; Bouvier &
Fischer, 1902; Fretter, 1964), but there is not
the multiplicity of the lateral teeth in that fami-
ly. There is no enlarged first marginal as in
fissurellids and some trochaceans. The radu-
lar morphology of Neomphalus is so different
from that of other archaeogastropods that it
offers no useful phylogenetic clues.

External Anatomy in Ventral View (Figs. 3A,
4A, 5B, 6): Shrinkage resulting from preserva-
tion has retracted the mantle margin away
from the growing edge of the shell, in most
specimens decreasing the diameter of the
animal by about a third (Fig. 3A). (In the fol-
lowing description of the ventral surface all
references to left and right sides are from the
normal dorsal aspect.)

Along the retracted mantle margin very fine
mantle tentacles in nearly retracted condition
are visible under high magnification on the
outer edge; these tentacles correspond to
grooves in the overhanging periostracum.
Larger projections correspond to the major
periostracal ridges on the shell.

The sole of the foot is oval except for its
obtusely pointed posterior tip. It projects
slightly on all sides, the anterior edge project-
ing to the greatest extent, where there is a
straight edge and a prominent transverse fur-

FIG. 3. Neomphalus fretterae. Holotype, USNM 784637, mature female attached to shell, dive 723, Oyster
Bed, maximum diameter 30.0, maximum height 7.8 mm. A) Ventral view, showing the contraction of the
body away from the shell margin and the projecting periostracum. The broad mid-ventral line on the neck is
an artifact from shrinkage, marking the position of the esophagus. B) Exterior view, anterior at top, showing

the periostracal ridges.

GALAPAGOS RIFT ИМРЕТ NEOMPHALUS 299

row, the opening of the anterior pedal mucous
gland.

A thin epipodial ridge encircles the foot and
extends forward on the ventral sides of the
neck, where it fades and disappears. Tenta-
cles are borne on this ridge only posteriorly.
Those on the right side occur on the posterior
third of the epipodium, the anteriormost con-
centrated on a projecting lobe bearing 4 to 9
short, stubby tentacles, with another two more
broadly spaced tentacles between this group
and the posterior tip of the foot. Tentacles on
the left side (the mantle cavity side) are more
limited, occurring only on the posterior fifth of
the epipodium, the anteriormost being in a
closely spaced group of 5 or 6, of which the
first is the shortest; beyond this group are two
longer and more broadly spaced tentacles.

The mantle cavity fills a space adjacent to
the foot along the entire left side of the animal,
extending posteriorly to a point opposite the
foot tip. Adjacent to the foot the mantle cavity
is closed and the gill axis shows through as a

supporting rod on the floor of the cavity. Adja-
cent to the neck the floor of the cavity is open
and the gill filaments arch over the neck. The
open portion of the mantle cavity extends over
the head to a corresponding point on the right
side.

Epipodial tentacles are prominent features
in archaeogastropods other than Pleuroto-
mariidae, Neritacea, and Patellacea. In no
other family is there a similar elaboration in
which they are entirely restricted to the posteri-
or region and bunched together.

The pedal mucous gland is prominent in
Pleurotomariidae, Scissurellidae and some
trochaceans but is lacking in Haliotidae and
Fissurellidae.

External Anatomy in Dorsal View (Figs. 4B,
5A): Upon removal of the shell the crescent-
shaped columellar muscle is exposed. It sur-
rounds the visceral mass except at the left
side. No portion of the mantle cavity is en-
veloped by the shell muscle. A slit in the ante-
rior portion of the muscle marks the position of

FIG. 4. Neomphalus fretterae. Mature female removed from shell, the ctenidium and its skeletal support on
the floor of the mantle cavity excised. A) Ventral view, showing the epipodial tentacles bunched along the
posterior sides of the foot, the obtusely pointed tip of the foot, and the opening of the anterior pedal mucous
gland. Oral lappets extend on either side of the mouth, ventral to the posteriorly directed cephalic tentacles.
B) Dorsal view, showing the efferent pallial vein in the mantle skirt, the food groove cutting diagonally toward
the mouth, the crescent-shaped shell muscle surrounding the visceral mass except at the left side. The
dorsal surface of the visceral mass is covered by the ovary on the right and the narrow, three-chambered
glandular gonoduct on the left. The triangular pericardial cavity is left of the posterior arm of the shell muscle,
containing the large, dark-appearing auricle on the left, and the smaller, lighter-appearing ventricle on the

right.

300 McLEAN

FIG. 5. Neomphalus fretterae. Mature male removed from shell. A) Dorsal view, showing the crescent-
shaped shell muscle surrounding the visceral mass, which is covered by the testis on the right and prostate
on the left. The mantle skirt is contracted and folded. The free tip of the ctenidium lies over the neck and the
filaments extend to the right. B) Ventral view, showing the enlarged left cephalic tentacle adjacent to the left
neck groove; other structures as in the female, Fig. 4A.

the interior shell ridge, which provides addi-
tional surface for muscle insertion.

The mantle skirt is relatively thin, apart from
a thickened margin. It extends laterally in all
directions; it is narrow to the right of the shell
muscle and broad to the left where it roofs the
mantle cavity, and broad anteriorly where it
overlies the gill filaments that extend to the
right above the neck.

The pallial vein is prominent in the mantle
skirt, having its origin in the right anterior re-
gion of the mantle skirt and running midway
along the roof of the mantle cavity on the left
side of the animal. It extends to the posterior-
most region of the mantle cavity, where it
enters the auricle.

The triangular pericardial cavity is bordered
on the right by the posterior arm of the shell
muscle, on the left by the mantle cavity, and
anteriorly by the visceral mass. The auricle is
elongate, lying within the left side of the peri-
cardial cavity; the shorter ventricle fills the
right side.

The right-dorsal portion of the visceral
mass is occupied by the gonad, entirely con-
cealing the digestive gland and stomach be-
neath. Tubules within both the ovary and
testis are visible externally, converging in both
sexes at the left anterior region. Males (Fig.
5A) have a large bilobed prostate gland left of
the testis; in females the glandular duct region
is narrower than the prostate of the male,
presenting a curved dorsal surface about
three times longer than wide (Fig. 4B). The
glandular duct of the female is comprised of
three separate chambers, as detailed in the
description of internal anatomy (Fretter,
Graham & McLean, 1981).

Aside from the unique arrangement by
which the shell muscle envelops only the
visceral mass and not the mantle cavity, the
dorsal position of the gonad is unusual; in
other rhipidoglossate limpets the gonad
shares the dorsal position with the digestive
organs.

Head and Neck (Figs. 3A, 4, 5, 6, 7): The

GALAPAGOS RIFT ИМРЕТ NEOMPHALUS 301

FIG. 6. Neomphalus fretterae. Left-ventral view of male specimen after cutting ventrally along the floor of the
mantle cavity adjacent to the foot and folding up the ctenidium, showing the enlarged left cephalic tentacle
adjacent to the left neck groove. The mouth is a vertical slit between the oral lappets. Arrow points to the

male genital opening.

neck is long, wide, and flattened, so that its
thickness is only about Ya the height of the
shell muscle. It lies at the level of the foot, the
space above filled by the ctenidium. The ante-
rior end of the head is blunt— nothing projects
beyond the base of the cephalic tentacle—a
snout is therefore absent.

The mouth is a recessed vertical slit at the
ventral anterior edge of the head. Some spec-
imens are preserved with the inner lips
closed, the mouth appearing as a slit between
the outer lips; in others the outer lips are part-
ed and the buccal mass, jaw, and radula pro-
trude.

The dorsal anterior region of the head is
continuous with a pair of posteriorly directed
cephalic tentacles. Eyes are lacking. In males
of all sizes the left cephalic tentacle is larger
than the right and may extend along the open-
ing of the mantle cavity for 24 the length of the
neck. In most females the left tentacle is the
same size or only slightly larger than the right
tentacle. One specimen was observed in
which the left tentacle was sufficiently large to
suggest that it was male, but it proved on
gonad inspection to be female; thus, tentacle
dimorphism is not fully reliable for sex deter-
mination.

The neck has lateral extensions or lobes on
both sides. The right neck lobe is simple and

flaplike, its connection to the neck defined
along most of its length by the food groove.
Anteriorly the food groove arcs across the
dorsal surface of the cephalic lobe, cutting
deeply toward a notch directly above the
mouth. The right neck lobe merges with the
base of the right cephalic tentacle anteriorly.
The left neck lobe borders the opening to
the mantle cavity and is comprised of two
ridges with a deep channel between. The
ventral ridge is straight and smooth, and the
dorsal ridge is somewhat more ruffled or con-
tracted (at least in preserved material). Ante-
riorly the ridges rise above the base of the left
tentacle and fade dorsally where the tentacle
emerges from the head. No direct groove
leads to the mouth. Posteriorly the channel
margins terminate against the foot side, below
the ventral opening to the mantle cavity.
The head and neck of Neomphalus are
highly modified in relation to filter feeding and
thus are not comparable to the head and neck
in other archaeogastropod limpets. Neck
lobes in trochaceans are considered to be for-
ward extensions of the epipodium, but this
seems not the case in Neomphalus because
the neck lobes are not continuous with the
epipodial ridge. The flattened head and neck
is more like that of the Calyptraeidae but ex-
hibits the following unique features: 1) the

302

posteriorly directed cephalic tentacles, 2) the
enlarged left tentacle of the male (which cer-
tainly has a copulatory function), 3) the dorsal
route taken by the food groove (in the
Calyptraeidae and all other filter-feeding
prosobranchs it passes beneath the right
cephalic complex rather than over it), 4) and
the depth of the left neck channel (the
Calyptraeidae have a left neck groove, but it is
shallow in comparison).

Mantle Cavity (Figs. 4, 6, 7, 9): The mantle
cavity lies over the head, as in most proso-
branchs, but differs from most in having its
closed portion extending to the left of the
cephalopedal mass, so that its total shape is
that of an inverted “L.” In most limpets there is
a horseshoe-shaped shell muscle that is open
anteriorly and fully envelops the posterior-
most extent of the mantle cavity, but in
Neomphalus the opening in the muscle en-
velops only the visceral mass, and the open-
ing is shifted 90° to the left. The anterior por-
tion of the shell muscle lies directly between
the neck and all of the visceral cavity. Access
to the right side of the animal is thereby un-
available to the mantle cavity organs normally
associated with the right side.

Structures within the mantle cavity can be
observed either by cutting into it ventrally be-

McLEAN

tween the base of the gill and the foot (the
mantle skirt folded up with the gill attached),
or by cutting dorsally to the right of the pallial
vein and the gill folded down.

The ctenidium (Fig. 8) fills the entire mantle
cavity. It is attached on the floor of the deep,
enclosed portion of the cavity and its free tip
extends beyond the ventral opening of the
Cavity to fill the entire space above the head. It
is bipectinate throughout, with long narrow
filaments of equal length on both sides of the
axis. There is no dorsal (afferent) mem-
brane—the attachment is entirely ventral (ef-
ferent). The thickened ventral axis continues
along the free tip, providing support for the
long filaments.

The gill axis within the closed portion of the
mantle cavity is placed so that afferent and
efferent vessels are aligned nearly vertically;
where the cavity opens ventrally the axis
makes a 120° bend to the right and turns to lie
flat. Here the two vessels are horizontally
aligned and the filaments from both sides of
the axis are directed over the neck. Water cur-
rents thus may pass through filaments on
both sides of the axis.

On a large specimen 190 separate leaflets
were counted on each side of the gill axis.
Those that emerge deep in the mantle cavity

FIG. 7. Neomphalus fretterae. Female specimen from left side after cutting the mantle skirt between the
visceral mass and the pallial vein; tips of ctenidial filaments excised to show the afferent side of the ctenidial

axis. Arrow points to the female opening.

GALAPAGOS RIFT LIMPET NEOMPHALUS 303

FIG. 8. Neomphalus fretterae. Ctenidium from specimen in Fig. 4, showing the close spacing and rounded
tips to the filaments and the bend to the right midway along the axis. Filaments that arise beyond the bend
terminate in a line coresponding to the position of the food groove where it traverses the neck.

are short and do not reach the opening. Fila-
ments arising closer to the bend are longer,
and those that emerge at the end are the
longest. Tips of all the filaments impinge upon
the food groove. On a large specimen the
longest filament measured 9mm in length
and 0.4mm in width throughout its length,
which was therefore 22 times the width, com-
parable to the figure of 26:1 given by Yonge
(1938) for Crepidula. Tips of the filaments are
rounded. The filaments are not easily sepa-
rated; a single filament cannot be removed
without tearing the adjacent filaments. The
cilia on the filaments and the skeletal rods
within are treated in detail by Fretter, Graham
& McLean (1981).

The food groove may be traced from the
posterior end of the right neck lobe to near the
innermost part of the mantle cavity, though
sometimes appearing as a ridge rather than a
groove. From the neck lobe it runs to the left
over the dorsal surface of the head-foot and
then backward, ventral to the anus, the genital
opening, the ciliated area alongside that in
females, and the kidney and _ pericardial
Cavity.

The osphradium consists of two elongated
patches of dark-staining sensory epithelium at
the base of the gill within the closed portion of

the mantle cavity behind the separation of the
free tip to the ctenidium. This position is com-
patible with the normal position of the
osphradium in aspidobranch gastropods, in
which it is located at the leading edge of the
efferent membrane that supports the free tip
to the ctenidium. In Neomphalus the efferent
membrane is thick and extends through the
free tip, so that the osphradium has to be
partitioned on both sides of the ctenidial axis
to retain its usual position.

The left kidney opening is a tiny pore deep
on the dorsolateral wall of the mantle cavity
slightly posterior to the ventral inhalant open-
ing and just within the anterior limb of the shell
muscle. In females the genital opening has
prominent rosette-shaped lips; from their
base a series of fine, ciliated ridges and
grooves runs posteriorly, dorsal to the food
groove, to the opening of the receptaculum
seminis. In males the opening is recessed,
and the lips curve forwards to form a groove
lying ventral to the rectum. The extreme left-
ward shift and considerable depth of the man-
tle cavity has the important consequence of
keeping the genital openings on the left side
of the body, unlike the condition in all other
single-gilled prosobranchs, in which the re-
productive functions are entirely performed at

304

the right side of the head. The displacement
of the genital opening to the left side explains
why it is the left rather than right cephalic
tentacle of the male that is modified as a
copulatory organ.

The rectum, upon emerging from the kidney
cavity at about the position of the genital
opening, is suspended dorsally in the mantle
cavity, running adjacent to the shell muscle.
The anus is positioned directly over the mid-
point of the neck. A rod of fecal material con-
tinues in a groove in the mantle skirt adjacent
to the shell muscle, which carries the fecal rod
to the right, where it can be expelled when the
shell edge is raised.

No distinct region in the mantle skirt can be
regarded as hypobranchial gland, although
scattered subepithelial gland cells are pres-
ent. This is in striking contrast to the promi-
nent ridged and convoluted development of
discrete left and right hypobranchial glands in
the pleurotomariids, haliotids and trochace-
ans. In these groups left and right hypo-
branchial glands are separated by the rectum
in the mantle skirt. In Neomphalus the rectum
does not traverse the mantle skirt. Hypo-
branchial gland development comparable to
that of Neomphalus occurs in the Fissurelli-
dae, in which gland cells are present in the

McLEAN

mantle skirt but do not form a discrete organ
with a folded surface.

The ctenidium of Neomphalus is unique
in the Gastropoda. It is the only ctenidium
bipectinate throughout its entire length in
which the filaments are elongate and the af-
ferent membrane is lacking. Its length and
mass is no doubt greater than that of any
other living gastropod. Only in bivalves may
the length of the gill be equal to that of the
animal. The afferent membrane is lacking in
one other family in the Archaeogastropoda—
the Pleurotomariidae. Pleurotomariid ctenidia
differ in being paired, the filaments not elon-
gated, the efferent membranes not thickened.
The pleurotomariid mantle cavity extends
even deeper than that of Neomphalus, past
the ctenidial origin.

Growth and Shell Ontogeny: Four small
specimens, having shell diameters of 1.7, 3.2,
3.8, and 4.0 mm, were collected on the sec-
ond expedition in February 1979. The shell of
the 1.7 тт specimen was mounted for SEM
examination of the aperture (Fig. 10C); the
3.2 mm specimen remains intact; the 3.8 mm
specimen was critical-point dried for SEM ex-
amination of the animal (Fig. 10D); and the
4.0 mm specimen was used for SEM study of
its exterior (Figs. 10A, B).

FIG. 9. Neomphalus fretterae. Juvenile shell of female, dive 733, Garden of Eden, diameter 7.0 mm. A)
Exterior, anterior at top, showing flat-lying coil of early whorls. B) Interior, anterior at top, showing abandoned
columella from the early coiled phase, the muscle scar and the shell ridge now positioned directly over the

base of the early shell.

GALAPAGOS RIFT LIMPET NEOMPHALUS 305

FIG. 10. Neomphalus fretterae. SEM views of early stages. A) Protoconch, maximum diameter 0.2 mm. B)
Oblique view of protoconch and first two postprotoconch whorls, same specimen as Fig. 10A. C) Basal view
of coiled juvenile shell 1.7 mm in diameter, showing the rudiment of the shell ridge, the rounded columellar
lip along which growth has stopped, and the encirclement by lip growth on the right 34 complete. D) Ventral
view of critical-point-dried juvenile attached to shell, shell diameter 3.8 mm, showing larval operculum
0.8 mm in diameter, the prominent opening of the anterior pedal mucous gland, jaws and other adult
features, except that the neck is short, the mantle cavity not open on the left and the gill filaments not in
evidence.

306 McLEAN

The critical-point dried specimen Fig. 10D)
shows the larval operculum attached vertical-
ly at the rear of the foot, its diameter 0.8 mm.
К has a tight central coil of 5 whorls and a
paucispiral final whorl. Epipodial tentacles,
jaws, the oral lappets, and the anterior pedal
gland are well developed. Major differences
from the adult are that the neck is relatively
short, the gill filaments are not visible, and the
mantle cavity opening ventral and left of the
neck is not apparent nor is the left neck
groove. Cephalic tentacles are laterally di-
rected. The larval operculum of Neomphalus
reaches a larger size and persists through
more advanced stages of development than
in limpets of any other family.

Neomphalus is also unique among limpets
in the manner in which it makes the transfor-
mation from a coiled juvenile to the adult shell
form. The transformation takes place in the
second postprotoconch whorl, and results
from cessation of growth of the columellar lip
and accelerated growth along the suture and
upper margin of the lip. A new suture is laid
upon the periphery of the Lamellaria-like shell
until the lip extends a full 360°. The stage at
which the process begins is not marked by a
line of transition on the external surface. This
transformation is nearly complete on the
1.7mm diameter specimen (Fig. 10C), in
which the columellar lip is rounded and the
base of the shell exposed, as yet uncovered
with callus deposits. The total cessation of
growth on the columellar lip is clearly indi-
cated in larger juvenile shells (Fig. 9B), in
which the old columella remains visible in the
apical position of the shell interior.

The transformation to the limpet form in-
volves a 90° shift in the orientation of the ani-
mal relative to the initial axis of coiling. Such a
change is inferred because the larval stage in
the 0.2 mm long protoconch would have the
orientation common to all veliger stages with
the head balanced relative to the axis of coil-
ing. Because the animals in all the small spec-
imens are oriented perpendicular to the plane
of the aperture, they must have completed
this 90° shift during the growth of the second
postprotoconch whorl, coinciding with cessa-
tion of growth on the columellar lip.

Cessation of coiling fixes the orientation of
the head and columellar muscle at an early
stage. The columellar muscle of the coiled
juvenile would be just inside the columellar lip;
the cessation of coiling forces the growing
muscle to emerge and assume a position on
the base of the shell, where it expands with

growth. The rudiments of the shell ridge are
apparent on the 1.7 mm specimen (Fig. 10C).

The cessation of growth along the basal
part of the columellar lip explains why the
columellar muscle does not form the encom-
passing horseshoe-shaped shell muscle of
most other limpets. In transitional forms be-
tween normally coiled trochids and auriform
limpet-like stomatellid trochaceans, the
columella is lengthened, as is the columellar
muscle. This expansion of the columellar
muscle along the left side (viewing the animal
dorsally) envelops the mantle cavity on the
left, producing, upon further reduction of coil-
ing, the horseshoe-shaped muscle that entire-
ly envelops the visceral mass posteriorly and
the mantle cavity anteriorly. In Neomphalus
the left arm of the muscle is not stretched
along an expanding columella and thus does
not envelop the mantle cavity on the left side.

Thus many of the unusual features of
Neomphalus can be traced to growth stop-
page on the juvenile columella, which halts
coiling and generates the limpet form, at the
same time preventing the mantle cavity from
being enveloped on the left side. The orienta-
tion of the animal relative to the columella and
axis of coiling is forced to change.

Shell ontogeny in the Calyptraeidae, re-
cently described by Fretter (1972), follows a
different course: the columellar lip of the
protoconch expands, altering the axis of coil-
ing, followed by the addition of a projecting
peripheral rim on all sides, producing the
limpet shell. Folds of the mantle produce the
calyptraeid septum by adding a flange to the
Original columella. Neomphalus differs in that
the limpet shell results from progressive
rather than simultaneous encirclement and
the old columella is completely abandoned. In
the calyptraeid the columellar muscle is
drawn out along the septum, retaining major
attachment points at both ends; hence the
calyptraeid has the horseshoe-shaped mus-
cle with its extremities at both sides of the
mantle cavity, as in most limpets. In the
Patellacea, Fissurellacea, and the neritacean
limpets, the horseshoe-shaped muscle re-
sults from fusion of the left and right mus-
cles; only minor changes in the orientation of
the animal relative to the axis of coiling are
involved.

Life habits

Neomphalus limpets live clustered near
and extending into the vents (Fig. 11), where

GALAPAGOS RIFT LIMPET NEOMPHALUS 307

they are in close association with the vesti-
mentiferan Riftia pachyptila Jones (1981).
Vent effluent at the Garden of Eden vent-field
has a maximum temperature of 17°C, in con-
trast to the ambient bottom temperature of
approximately 2°C. Vent effluent contains
hydrogen sulfide and is reported as anoxic
above 10°C, but presumably mixes sufficient-
ly with oxygenated ambient water to sustain
the limpets. Current flows of 2 to 10 cm/sec
have been measured (all data from Corliss et
al., 1979, p. 1082). The limpets are often in
contact and some are positioned on the shells
of others, as shown on the large fragment of
pillow basalt from the Garden of Eden (Fig.
12A). The broad anterior surfaces of the
limpets on the boulder (Fig. 12A) are facing in
different directions, indicating that there was
no orientation with reference to currents.
Neomphalus may attach to the tubes of Riftia
(Fig. 12B), although there is no indication of
this in Fig. 12A.

Neomphalus is primarily sedentary; the
shell margin is irregular, evidently conforming
to a particular site. Those attached to other
shells leave no attachment scars nor cause

any damage to the periostracum of the lower-
most shell. The periostracum should provide
a seal along the shell edge that would protect
it from the claws of the brachyuran crab
Bythograea thermydron Williams (1980), a
potential predator at the Galapagaos Rift. The
foot of Neomphalus is sufficiently muscular for
locomotion. Some motility would be required
for the mating we deduce from the anatomy
(Fretter, Graham & McLean, 1981).

Suspended bacterial cells in the rift-vent ef-
fluent have been measured in the range of 5
x 105 to 106 per ml (Karl et al., 1980) during
the January 1979 expedition; Corliss et al.
(1979) reported a count of 108 to 109 bacterial
cells per ml in preserved samples from the
1977 expedition. Thus there is a sufficient
source of suspended food to sustain large
populations of filter-feeding animals. Mats of
microorganisms also develop on shell or rock
surfaces in the vicinity of the vents (Jannasch
& Wirsen, 1981), providing a source of food
for limpets that feed by grazing.

Gut contents in Neomphalus suggest that
feeding is a combination of grazing and filter
feeding (Fretter, Graham & McLean, 1981).

FIG. 11. Oyster Bed vent-field, dive 726, showing the vestimentiferan, Riftia pachyptila, the brachyuran crab
Bythograea thermydron in upper center, the galatheid crab at lower left, and numerous Neomphalus
fretterae on all exposed surfaces.

308 McLEAN

FIG. 12. A) 72 Ib fragment of pillow basalt from dive 733, Garden of Eden, photographed on deck of support
ship, showing Neomphalus in place and tubes of the vestimentiferan, Riftia. В) Tube of Аа with attached
Neomphalus in place, from 1979 expeditions, dive number unknown.

Wear on the rachidian and lateral teeth (Fig.
2D) provides additional evidence that the
radula is used for grazing. The prominence of
the jaw and buccal development and retarda-
tion of the gill development in juvenile speci-
mens (Fig. 10D) suggests that grazing is the
exclusive feeding mode of young stages. A
retention of the grazing capacity and a com-
bination of the two feeding modes in adults is
therefore not surprising.

Sectioned specimens examined by Fretter,
Graham & McLean (1981) showed ripe
gonads with gametes in all stages of develop-
ment, indicating that reproduction is a constant
process throughout the year, in agreement
with observations that in the absence of
seasonal stimuli, most deep-sea invertebrates
spawn throughout the year (Rokop, 1974;
Rex et al., 1976).

The reproductive anatomy of Neomphalus
indicates that copulation must take place, that
sperm are stored in a receptaculum seminis,
that fertilization probably takes place in the

proximal arm of the genital duct, and that fer-
tilized eggs receive a coating of jelly-like ma-
terial before extrusion from the distal arm of
the genital duct (Fretter, Graham & McLean,
1981). Egg capsules have not been collected;
thus, the next step is unknown and it is un-
certain whether individually encapsulated
eggs are released freely or attached to the
substratum. A sufficient number of females
have been collected to rule out the possibility
that developing young are brooded under the
shell. Egg masses have apparently not been
found attached to the boulders from which the
specimens were collected. The free release of
coated eggs therefore seems most likely.

A coated egg, upon expulsion from the
mantle cavity might settle in a crevice or per-
haps become entangled by the byssal threads
of the rift-vent mytilid. A postprotoconch larval
shell with a sharp transition preceding the on-
set of adult sculpture is lacking, indicating that
there is по planktotrophic veliger stage
(Shuto, 1974; Robertson, 1976). Plankto-

GALAPAGOS RIFT ИМРЕТ NEOMPHALUS 309

trophic veligers are unknown in archaeo-
gastropods (Fretter, 1969) and Neomphalus
is no exception. Direct development through
the trochophore and veliger stages probably
takes place within the egg coating; crawling
juveniles would emerge. During the growth of
the first and second postprotoconch whorls,
the juvenile Neomphalus would be active but
would remain in crevices or among the byssal
thread of the mytilids. When the transforma-
tion to the limpet is completed by the end of
the second postprotoconch whorl, the limpets
would take up a more sedentary, primarily
filter-feeding existence where exposed to the
strong flow of the rift-vent effluent. Those
juvenile specimens received were recovered
from residue samples associated with the
mussels. The mature mussels live in a zone
further away from the vents; thus there is
some evidence that the early life of the juven-
ile takes place away from the vents.

The hypothesized course of development
should enable the continuation of populations
at each vent site, but it does not account for a
mechanism of dispersal to more distant vent
sites. Individual vent fields have been postu-
lated to have a rather brief, ephemeral ex-
istence of several hundred years, ‘necessitat-
ing the colonization of the new vent sites that
emerge along the spreading sea floor.

Unlike Neomphalus the mytilid from the
Galapagos Rift seems to have an effective
dispersal mechanism. Because if has a well-
defined larval shell, Lutz et al. (1979) inferred
that there is a planktotrophic larval stage
capable of long-range dispersal via bottom
currents, its metamorphosis indefinitely de-
layed because of lower metabolic rates at
ambient bottom temperatures. For Neom-
phalus, however, the colonization of new
vents may be a matter of passive transport via
larger, as yet unknown animals that may
move between the springs.

DISCUSSION

As discussed by Fretter, Graham & McLean
(1981), the neomphalid anatomy is an extra-

ordinary combination of archaeogastropod
and mesogastropod characters combined
with some unique features. That it is a highly
modified and specialized archaeogastropod
cannot be doubted, for it has such primitive
archaeogastropod characters as a rhipido-
glossate radula, а bipectinate ctenidium,
epipodial tentacles, and the anterior loop of
the intestine. Its features at the mesogastro-
pod level of organization include the nearly
complete reduction of the right pallial com-
plex, a monotocardian circulatory system,
expansion of the left kidney and formation of a
nephridial gland, a copulatory organ in the
male, and glandular gonoducts in both sexes.
Unique features include the split osphradia,
absence of a snout, dorsal position of the food
groove, posteriorly directed cephalic tenta-
cles, the enlargement of the left tentacle to
form a copulatory organ, and an unusually po-
sitioned receptaculum seminis in the female.

Fretter, Graham & McLean (1981) discuss
the leftward rotation on the anterior-posterior
axis and the 90° of further torsion, so clearly
shown in the placement of the internal organs,
that accounts for many of the unusual aspects
of the anatomy. These shifts and rotations
can be understood as resulting from the early
ontogeny, as described here, in which growth
stops along the columella, forcing the colu-
mellar muscle to emerge to the base of the
shell, and changing the orientation of the ani-
mal from its initial axis of coiling. Can it be
shown that some of the features of this ontog-
eny occur in the evolutionary history of
Neomphalus? Although Neomphalus fret-
terae is the only known member of a group
that can be assigned to no family, superfamiy,
or suborder with living representatives, its
evolutionary history can be sought in the fossil
record, even though no fossil record of the
genus itself has been found.3

Argument for an Archaic Origin

The neomphalid ctenidium is a departure
from other gastropod ctenidia. It is a mor-
phological innovation, an effective adaptation
for filter feeding. The course of evolution is

3Four poorly known Devonian genera, Procrucibulum, Paragalerus, Progalerus, and Protocalyptraea, have names that
imply some similarity to the shell form of calyptraeids. An affinity of these genera to the Calyptraeidae, which appeared in the
Cretaceous (Hoagland, 1977) has to be ruled out. However, these genera are of interest as possible precursors to the
Neomphalidae. Except for Paragalerus, drawings of reconstructed shells were illustrated in the Treatise (Knight et al., 1960).
Each genus is known only from the type-species (Yochelson, personal communication), holotypes of which were described
and illustrated by Knight (1941). The first three are represented by internal molds that lack information about protoconchs
and muscle scars. Protocalyptraea is based on a small incomplete specimen (see also Linsley et al., 1978: 111), in which the
peripheral frill would seem to preclude it as a precursor for Neomphalus. Affinity of these genera with the Neomphalidae
cannot be completely dismissed, but it cannot be discussed further until better material is known.

310

marked by adaptive radiations, proliferations
of new taxa following the introduction of suc-
cessful morphological innovations (Simpson,
1953; Stanley, 1979). Thus, the neomphalid
ctenidium should either have given rise to ex-
perimentation or be an end result of experi-
mentation that has already taken place. Be-
cause Neomphalus has many unique and
very specialized features and because it oc-
curs in an environment with many limiting
parameters, it surely must represent a single
twig of a larger branch in a group having the
same ctenidial structure. №5 predecessors
need not be limpets, for limpets are evolution-
ary dead ends, giving rise to adaptive radia-
tion within a family or superfamily, but not
serving as raw material for the further evolu-
tion of higher categories.

The limpet form has been derived from
coiled predecessors with some frequency
in gastropods. Among archaeogastropods,
mesogastropods, opisthobranchs, and pul-
monates there are many families of limpets.
One example is known in a siphonostomate
neogastropod—that of Concholepas. Except
for the docoglossate patellaceans, for which a
convincing derivation has never been offered,
the limpet families are closely related to fami-
lies or superfamilies having regular coiling,
particularly those in which the shell aperture is
holostomate rather than siphonostomate.

In some families or superfamilies—for ex-
ample the trochacean Stomatellidae—there
are limpet derivatives in which the entire pro-
gression from a trochiform to auriform and to a
limpet shell form is represented. In others, like
the Patellacea and the Calyptraeidae, there
are no clues as to the shell form of the closest
relatives. In these groups the derivation may
have been sudden, in a process of paedo-
morphosis, a phylogenetic derivation in which
reproductive maturity is attained in a stage
before the development of adult characters
(see Gould, 1968; Stanley, 1979). Normal
adult coiling does not take place; rather, shell
growth expands the aperture of the juvenile
Shell. In each case the limpet’s anatomy,
though modified by loss of coiling, retains a
sufficient number of characters common to its
ancestor (shared primitive characters) to
permit its taxonomic placement. The external
features of any limpet animal—for instance
the modifications of the head for its generally
constant retention under the protective shield
of the shell-have some similarity from one
family to another, but there are so many di-
verse anatomies represented in limpet fami-

McLEAN

lies that it is apparent that the form itself im-
poses few constraints upon the internal
anatomy. Thus, the major features of a lim-
pet’s anatomy must be a reflection of primitive
characters in its coiled predecessor.

In the absence of a living coiled group with
anatomy comparable to that of a particular
limpet, one may hypothesize the anatomy of
the coiled predecessor, basing the recon-
struction around the characters displayed by
the limpet that are assumed to be primitive
and not a consequence of the limpet mode.

Although the ctenidial filaments of Neom-
phalus are highly modified for filter feeding,
the basic configuration of the neomphalid gill
—aspidobranch with afferent attachment
lacking—is a character that would be shared
with the coiled predecessor. The only com-
parable condition in which an aspidobranch
gill lacks an afferent membrane occurs in the
Pleurotomariidae, in which the gills are
paired. The Pleurotomariidae are regarded as
the most primitive living gastropods. The
superfamily Pleurotomariacea has a fossil
record that is continuous from the Upper
Cambrian. The possible affinity of Neomphal-
us to the extinct groups contemporary with the
early pleurotomariaceans must be consid-
ered.

Although the subordinal classification of
archaeogastropods proposed by Cox &
Knight (1960) for use in the Treatise (Knight et
al., 1960) is due for modification, all of the
major divisions they recognized are traceable
to the early Paleozoic, the only remaining
doubt being that surrounding the appearance
of the Patellina—whether early or late in the
Paleozoic. Most of the living archaeogastopod
families made their appearance by the early
Mesozoic, well in advance of the burst of evo-
lution in the Neogastropoda during the
Cretaceous. If all other high-level, subordinal
origins and initial radiation of archaeogastro-
pod taxa took place in the Paleozoic, it is logi-
cal to assume that the subordinal distinction in
Neomphalus also had a Paleozoic origin.

Excluding the living and fossil groups for
which there is reasonable certainty that the
gill condition was dibranchiate, and excluding
the neritaceans, a completely divergent line
(Fretter, 1965), for which the fossil record is
well understood, those extinct, conispirally
coiled archaeogastropods that may have had
a unibranchiate mantle cavity were placed by
Knight et al. (1960) in two of the suborders of
Cox & Knight—the Macluritina and the
Trochina. In that classification the extinct

GALAPAGOS RIFT ИМРЕТ NEOMPHALUS 311

superfamilies in the suborder Macluritina
were the Macluritacea and Euomphalacea; in
the suborder Trochina there were four extinct
superfamilies: Platyceratacea, Microdomata-
cea, Anomphalacea, and Oriostomatacea. In
addition there were five superfamilies of
“doubtful subordinal position,” for which sin-
gle gills were likely: the Clisospiracea,
Pseudophoracea, Craspedostomatacea,
Palaeotrochacea, and Amberleyacea. These
represent major evolutionary lines for which
there is no direct information about their anat-
omies. Implicit in the ranking of these groups
as families and superfamilies is the assump-
tion that they had anatomical differences
comparable to those that distinguish the living
families for which the anatomy is known. Was
there in fact as great a diversity in anatomies
as is implied by the number of available
supraspecific categories?

In the Trochacea, the only superfamily of
the suborder Trochina recognized as living,
many authors (Risbec, 1939, 1955; Yonge,
1947; Clark, 1958; Graham, 1965) have found
the structure of the ctenidium to be virtually
identical among species examined in all
trochacean families, including the Trochidae,
Stomatellidae, Turbinidae, and Phasianelli-
dae.4 In its most familiar condition the
trochacean ctenidium has a free tip with a
strong ventral skeleton and gill leaflets of
equal size on both sides of the axis. Posterior
to the free tip about 23 the length of the
ctenidium is supported by both dorsal afferent
and ventral efferent membranes (Fretter &
Graham, 1962, figs. 53, 170). Here the leaf-
lets on the right side of the axis, where there is
more space, are larger than those of the left
side, which are confined in a deep narrow
chamber (see Yonge, 1947, fig. 25). The
number of leaflets in the deepest reaches of
this chamber may be reduced compared to
those on the right. There are two modifica-
tions of this basic plan, that of Umbonium
(Fretter, 1975) in which the entire gill is
monopectinate and fused to the mantle wall
throughout its length, and that noticed in
Margarites (Fretter, 1955: 161) in which “the
long aspidobranch gill lies freely in the mantle

cavity, and both afferent and efferent mem-
branes are short... .” | have found that this
latter condition is true of several other
trochacean groups, as will be discussed fur-
ther in a separate paper (McLean, in prepara-
tion).

All three of these different expressions of
the trochacean gill have in common the trans-
verse pallial vein, an additional conduit to the
afferent ctenidial vessel, requiring at least a
short afferent membrane for support (except
in Umbonium). The left gill of the trochacean
differs in this way from the left gill of the
pleurotomariid, which lacks the transverse
pallial vein and thereby has far less efficient
circulation to the ctenidium. The trochacean
pallial complex has evidently been highly ef-
fective from its inception, for the Trochacea
are the most successful of living archaeo-
gastropods in numbers of extant species and
diversity of habitat. The extent of adaptive
radiation possible for a group with the
trochacean pallial complex has probably been
attained.

The anatomical similarity of trochacean
families is a remarkable fact, considering the
diversity of shell shape, shell structure, and
opercular structure. The close anatomical
relationships between families with nacreous
interiors and the Skeneidae and Phasianelli-
dae, in which the primitive nacre is replaced
by lamellar aragonite, would seem to belie the
frequently emphasized principle that shell
structure is a conservative character (for
example, Batten, 1972, 1975). It is entirely
possible that many of the extinct groups could
have had anatomies that would place them in
the Trochacea. The diversity of shell form in
the Trochacea is broad enough to encompass
the extremes of shell shape in some,
though not all, of the extinct superfamilies.
The problem can be approached by asking
how the shell features in extinct groups would
impose functional constraints upon their
anatomies.

The Trochacea are dated from the Triassic
by Knight et al. (1960: 247), but there is no
clear argument in the literature to exclude
many older extinct families or even super-

4The Skeneidae, doubtfully considered trochaceans a short time ago (Fretter & Graham, 1962: 618), are now shown to have
trochacean anatomy (Fretter & Graham, 1977: 81). | have examined the pallial complex in Liotiidae and have found a gill
condition like that described by Fretter (1955: 161) for Margarites. The Seguenziidae, however, despite the nacreous interior
and modified rhipidoglossate radula (Bandel, 1979) have, in addition to the right subocular peduncle often occurring in
trochids (see Crisp, 1981), a very large penis behind the right cephalic tentacle, as well as a fully monopectinate ctenidium
(personal observation on a preserved specimen). This suggests, pending study of the internal anatomy, that mesogastro-
pod-like specializations in the reproductive system have been attained and that a superfamily apart from Trochacea may be

required.

312 McLEAN

families from the Trochacea. In Appendix 1, |
show that a Permian group assigned to the
Craspedostomatacea cannot be distin-
guished from extant trochacean Liotiidae,
which suggests that the trochacean anatomy
was well established in the Paleozoic.

The trochaceans share so many characters
with the living Pleurotomariidae—nacreous
interior, left kidney a large papillary sac, spiral
caecum in the stomach, paired auricles, skel-
etal rods in the ctenidial filaments, large
paired hypobranchial glands—that their deri-
vation from a pleurotomariacean stock is read-
ily understood (Fretter, 1964, 1966). However,
the pallial condition of the Trochacea with the
transverse pallial vein is not what would re-
main after a change amounting to little more
than the loss of the right ctenidium.

Between the dibranchiate Pleurotomariacea
and the unibranchiate Trochacea, Neom-
phalus is the only living form that is transi-
tional in having a single bipectinate ctenidium
with supporting skeletal rods in the filaments,
no afferent support, and thereby no additional
afferent conduits to the auricle.5 Except for its
modification for filter feeding, the neomphalid
ctenidium represents what remains after the
loss of the right ctenidium of a pleurotomaria-
cean. With or without the filament elongation,
the pallial condition of Neomphalus, if it ex-
isted in a coiled shell, would be an alternative
anatomy that could provide an explanation for
the anatomies of some extinct Paleozoic
groups. This pallial complex, like the trocha-
cean pallial complex, would also impose con-
straints upon the diversity attained by adap-
tive radiation in some extinct groups.

As discussed in the section that follows,
paleontologists have recently hypothesized
that filter feeding was the likely feeding mode
in the extinct Macluritacea and Euomphala-
cea. The neomphalid ctenidium provides a
mechanism by which these archaic gastro-
pods could have been filter feeders. Apart
from the ease with which the neomphalid
ctenidium may be invoked to account for filter
feeding, there are clues about the coiled
predecessor in the shell, for Neomphalus has
a coiled phase in its first postprotoconch
whorl. The ontogeny of Neomphalus provides
clues to its phylogeny. My theory is that the
Neomphalidae are limpet derivatives of the
Euomphalacea.

The Euomphalacea, along with the Maclu-
ritacea, have been regarded as comprising
the archaeogastropod suborder Macluritina
(Knight et al., 1960). Yochelson (manuscript)
provides arguments that a close affinity be-
tween the two groups is no longer tenable and
that subordinal separation can be justified. A
suborder Euomphalina is therefore necessary
to include the superfamily Euomphalacea
and the new superfamily Neomphalacea.
Formal proposal of the new suborder is given
in the concluding section of this paper. The
Macluritacea are discussed further in Appen-
dix 1.

In the section that follows, | summarize
what is known of the Euomphalacea, with a
particular effort to contrast the group with the
Trochacea. This is followed by a review of the
recent work that proposed a filter-feeding
mode for the Euomphalacea.

Current Understanding of the Euomphalacea
(Fig. 13)

Diagnosis: Shell low-spired to discoidal,
broadly umbilicate, some genera open-coiled;
coiling dextral, some discoidal genera with the
coiling rising slightly above the apical whorl
rather than descending below; peritreme
complete, upper lip trace usually sinuous but
not with slit or selenizone; aperture radial, its
plane passing through the coiling axis;
operculum (where known) calcified, external
pattern multispiral, inner surface with adventi-
tious layers.

Included Families: Euomphalidae de
Koninck, 1881 (Middle Ordovician to Trias-
sic); Euomphalopteridae Koken, 1896 (Siluri-
an); Oriostomatidae Wenz, 1938 (Upper Silu-
rian to Lower Devonian); Omphalocirridae
Wenz, 1938 (Devonian); Omphalotrochidae
Knight, 1945 (Devonian to Upper Triassic);
Weeksiidae Sohl, 1960 (Triassic to Cretace-
Ous).

The above diagnosis reflects an altered
concept of the Euomphalacea, which is con-
sistent with the paleontological literature that
has appeared since the last attempt at full
classification by Knight et al. (1960). They
recognized three constituent families (Heli-
cotomidae, Euomphalidae, and Omphalo-
trochidae) in contrast to six recognized earlier
by Wenz in 1938 (Euomphalidae, Omphalo-

SA short afferent membrane is present in both neritaceans and the acmaeid patellaceans; both groups also differ from the
Pleurotomariidae is lacking skeletal rods in the ctenidial leaflets (Yonge, 1947; Fretter, 1965). The cocculinid gill is not

bipectinate and there are no skeletal rods (Thiele, 1903).

GALAPAGOS RIFT LIMPET NEOMPHALUS 313

FIG. 13. Euomphalacean shells. A) Euomphalus pentangulatus J. Sowerby, 1814, Carboniferous (Euom-
phalidae), х0.9. В) Straparollus laevis (Archiac & Verneuil, 1842), Devonian, with attachment scars for shell
fragments (Euomphalidae), x 1.5. С) Amphiscapha reedsi (Knight, 1934), Pennsylvanian (Euomphalidae),
x 1.1. D) Serpulospira centrifuga (Е. A. Roemer, 1843), Devonian (Euomphalidae), x 1.1. E) Oriostoma
coronatum Lindström, 1884, with operculum (identified by Lindström to genus) in lateral view, Silurian
(Oriostomatidae), x 1.7. Е) Beraunia docens (Perner, 1903), Silurian (Oriostomatidae), x 1.1. С) Euom-
phalopterus alatus (Wahlenberg, 1821), Silurian (Euomphalopteridae), x0.6. H) Omphalotrochus whitneyi
(Meek, 1864), Permian (Omphalotrochidae), x 1.1. |) Weeksia lubbocki Stephenson, 1941, Cretaceous
(Weeksiidae), x 1.7. After Knight et al. (1960), except operculum in E, after Lindstrom, 1884, and С, after

Linsley et al., 1978.

cirridae, Platyacridae, Cirridae, Oriostomati-
dae, Poleumitidae, and Macluritidae). Two
recognized by Wenz—the Omphalocirridae
and Oriostomatidae—are now returned to the
list. Of the other families recognized by Wenz,
Platyacridae and Cirridae are here regarded
as trochacean (see Appendix 2), Poleumiti-
dae is synonymous with Euomphalidae
(Knight et al., 1960) and Macluritidae is dis-

cussed in Appendix 1. In the absence of an
overall revision of the Euomphalacea, the im-
portant changes since 1960 may be sum-
marized as follows:

Omphalocirrus was regarded by Wenz
(1938) as a sinistral euomphalacean, but by
Knight et al. (1960) as macluritacean; Yochel-
son (1966) returned it to the Euomphalacea
(Euomphalidae) as a dextral form with the

314 McLEAN

spinose projections on the under rather than
the upper side; Linsley (1978a) independently
proposed a family Omphalocirridae to include
also the genus Liomphalus (Fig. 14), which
lacks the spinose projections, neglecting to
note that Wenz (1938) had previously pro-
posed the family.

Euomphalopterus (Fig. 13G) had been
treated as pleurotomariacean, until its periph-
eral frill was no longer regarded as the site of
a selenizone by Linsley et al. (1978), who
transferred its family to the Euomphalacea.

Oriostoma (Fig. 13E), with its multispiral
operculum and nacreous interior, was given
family and superfamily status in the Trochina
by Knight et al. (1960); Linsley (1978a) sug-
gested the transfer of Oriostomatidae to the
Euomphalacea, in which it had been previ-
ously placed by Wenz (1938). Opercular
characters support this assignment, as dis-
cussed in the section that follows.

Euomphalid genera of the Mesozoic in-
cluded by Knight et al. (1960) require further
attention: some may need to be reassigned to
the Trochacea. Зо! (1960) proposed the
euomphalacean family Weeksiidae for three
biangulate, discoidal genera—Weeksia (Fig.
131), Discohelix, and Amphitomaria—differing
from euomphalids in having a prosocline up-
per whorl surface. He also noted that Hippo-
campoides is a magilinid (i.e., coralliophilid). |
assign Anosostoma, which had a greatly ex-
panded final lip (Fig. 18B) to the trochacean
Liotiidae in Appendix 2; no genera with ex-
panded apertures remain in the Euomphala-
cea.

Yochelson (manuscript) removes Lesueu-
rilla (Fig. 15A) and other genera with a slit or
slit-like feature on the upper lip to the Pleuro-
tomariacea, and suggests that all such gen-
era should be reconsidered. Rohr & Smith
(1978) have treated Odontomaria (Fig. 15C)
as pleurotomariacean. | propose that Helico-
toma (Fig. 15D) with its elevated slit be in-
cluded in this transfer, thereby removing the
Helicotomidae of Knight et al. (1960) from the
Euomphalacea. Transfer of such genera to
the Pleurotomariacea is in essence a return to
the classification of Wenz, who associated
them with the raphistomatid pleurotomari-
aceans.

The Euomphalidae have been reduced
since 1960 by the removal of groups men-
tioned above. The content of the Omphalotro-
chidae (Fig. 13H) remains unchanged.

It is beyond the scope of this review even to

estimate the number of euomphalacean taxa.
Additional genera have been proposed since
1960, and there are several entries per year
in the Zoological Record pertaining to the
group. In the monographic series on Permian
gastropods of the southwestern United States
(Yochelson, 1956, 1960; Batten, 1958), 45
bellerophontacean species, 32 pleurotomari-
acean species, and 31 euomphalacean spe-
cies were treated. All the other archaeogas-
tropods (Patellacea, Trochonematacea,
Pseudophoracea, Anomphalacea, Craspedo-
stomatacea, and Platyceratacea) together
totaled only 21 species. It is therefore clear
that the Euomphalacea comprised a major
share of the Paleozoic gastropod fauna.

Shell characters: Shell structure has here-
tofore been an important part of the diagnosis
for the Euomphalacea, but it is omitted here
because the admission of the nacreous Orio-
stomatidae (Lindstrom, 1884; Knight et al.,
1960) changes the previous concept that the
Euomphalacea were entirely non-nacreous.
As discussed above, the inclusion of families
with different shell structure is currently ac-
cepted in the Trochacea. Thus, the inclusion
of nacreous and non-nacreous families in the
Euomphalacea is not without precedent.

Boggild (1930: 301), in his classic survey of
the shell structure of mollusks, reported on
the Euomphalidae as follows: “In the shells of
this old family the aragonite is, of course,
never preserved but it seems to have existed
Originally. In most members examined by me
there is a prismatic layer which is sometimes
rather regular and which indicates that the
shell, in such instances, must have pos-
sessed an upper calcitic layer.” Knight et al.
(1960: 189) essentially repeated Boggild's
remarks in their superfamilial diagnosis.

The calcitic layer need not have great taxo-
nomic significance, for Водана (1930: 298)
noted that it “must be said to be a rather ac-
cidental element,” for it occurs “in a great
number of families,” and may be lacking alto-
gether in some genera within families where it
is otherwise known.

Shell structure would be an extremely use-
ful character in archaeogastropod classifica-
tion if it were always possible to determine the
Original structure of fossil shells. Little can be
said of most Paleozoic and Mesozoic genera
and nothing can be established for those of
the Cambrian and Ordovician. Presumably,
as in the Trochacea, nacreous interiors would
be primitive in the Euomphalacea, persisting

GALAPAGOS RIFT ИМРЕТ NEOMPHALUS 315

only in the family Oriostomatidae, a group un-
known past the Devonian.6

Although the range of possible shell forms
in the Trochacea overlaps that of the Euom-
phalacea (see Appendix 2), the euom-
phalaceans are generally lower spired. Some,
like the genus Serpulospira (Fig. 13D), are
open-coiled, defined by Yochelson (1971:
236) as “shell forms that fail to have some or
all of the whorls in contact but that do not
obviously deviate from logarithmic factors in
rate of coiling.” Open coiling occurs with
some frequency in the Euomphalacea, but in
a review of living forms that are open-coiled,
Rex & Boss (1976) reported no trochaceans
with this mode of coiling. |

The diagnosis for Euomphalacea given
here omits reference to the mode of coiling as
either orthostrophic or hyperstrophic, as in
Knight et al. (1960). Hyperstrophic coiling was
defined by Cox in Knight et al. (1960: 131) as:
“dextral anatomically, but shell falsely sinis-
tral... .” This is a concept easily understood
in conspirally coiled forms in which there is FIG.
dextral anatomy within a sinistral shell, as di-
agrammed by Cox in Knight et al. (1960: 111)
for the ampullariid genus Lanistes,’ but it is
here (on the advice of Yochelson) considered
as an inappropriate term to describe the coil-
ing in such discoidal euomphalacean genera
as Beraunia (Fig. 13F), Amphiscapha (Fig.
13C) and Liomphalus (Fig. 14), in which the
coiling rises slightly above the apex instead of
below it. Living gastropods that are anatomi-
caly dextral have an operculum with a coun-
terclockwise spiral on the external surface

14. Liomphalus northi (Etheridge, 1890),
Devonian, Lilydale Limestone, Lilydale, Victoria,
Australia. Showing the omphalocirrid operculum in
place and coiling differences attributed to sexual
dimorphism by Linsley (1978a). A) Apertural view of
specimen thought to be an immature female, di-
ameter 20 mm, coiling essentially orthostrophic. B)
Oblique apical view of specimen considered a ma-
ture male, diameter 75 mm, operculum in place,
coiling “hyperstrophic.” Photos courtesy В. М.
Linsley, specimens in the National Museum of
Victoria.

this and similar “hyperstrophic” genera for

(Pelseneer, 1893; Robertson & Merrill, 1963).
Opercula with a counterclockwise spiral are
known in such euomphalacean genera as
Liomphalus (Fig. 14), providing the evidence
generally accepted by paleontologists that

which opercula are unknown were anatomi-
cally dextral.

“Hyperstrophic” coiling has been used as а
generic-level character in some members of
the families Euomphalidae, Omphalocirridae

6Quinn (1981) has suggested that the nacreous Seguenziidae (see also Bandel, 1979) could have been derived from the
Omphalotrochidae, a family here included in the Euomphalacea. Because nacre is unknown in the Omphalotrochidae, such
a derivation would require the unlikely reversion to nacre.

7Hyperstrophy is known in two living mesogastropod families—in the larval stages of architectonicids and in the African
ampullariid genus Lanistes (see Wenz, 1938). In architectonicids it is normally limited to the planktotrophic veliger stage
(Robertson, 1964), although rare abnormal specimens have been found in which hyperstrophy persists in the adult (Robert-
son & Merrill, 1963). Normally the coiling changes to orthostrophic in the first teleconch whorl. In Lanistes it is apparent that
these moderately high-spired forms carry the shell directed to the left rear as in sinistral gastropods, but that water currents
move in the mantle cavity from left to right as in dextral gastropods (Lang, 1891: 368, fig. 21, copied in part by Cox in Knight
et al., 1960, fig. 67). Andrews (1965: 71) studied Lanistes and noted that its mantle cavity is deeper than that of orthostrophic
members of the family, but she did not discuss the functional advantage of hyperstrophy in Lanistes. Hyperstrophy raises
some questions, for, according to descriptions of torsion (Crofts, 1955), the normal course of development leads to dextral
orthostrophic coiling. Crofts showed that in the archaeogastropods Haliotis, Patella, and Calliostoma, the first phase of
torsion involves a delayed development of the left compared to the right post-torsional retractor muscle, which imposes an
immediate asymmetry upon the protoconch, causing the direction of coiling to proceed in the usual dextral manner. п
sinistral gastropods the anatomical sinistrality may be traced to the first stages of cleavage, as recently reviewed by Verdonk
(1979). Discussions of torsion (Lever, 1979, and references therein) make no mention of hyperstrophy. How hyperstrophy in
architectonicids and Lanistes can follow torsion is worthy of further investigation.

316

and Oriostomatidae. Linsley (1978a) consid-
ered that the four omphalocirrid species he
studied showed sexual dimorphism—a rea-
sonable conclusion based on the equal num-
bers of supposed male and female morpho-
types in each species. Those he interpreted
as females (Fig. 14A) tended to have 150-
strophic to orthostrophic coiling, in contrast to
the decidedly “hyperstrophic” males (Fig.
14B). This intraspecific variability in coiling
direction indicates that there was no anatomi-
cal difference between orthostrophic and
“hyperstrophic” euomphalaceans.

There are no families or genera in the
Euomphalacea in which there is a thickened
final lip or abrupt change in coiling direction,
as in the Trochacea (see Appendix 2).

The diagnosis for the Euomphalacea in
Knight et al. (1960, p. 189) included the provi-
sion: “commonly with channel presumed to
be exhalant occupying angulation on outer
part of upper whorl surface.” Yochelson
(manuscript) now notes that most euom-
phalaceans do not have a prominent shoulder
and that in those that have an angulation the
shell is thickened in that area and there is no
interior channel to be regarded as an exhalant
route. Thus, this provision of the diagnosis is
no longer included. It is to be noted that the
growth line on the upper lip of many euom-
phalaceans is often sinuous and opisthocline,
as in Omphalotrochus (Fig. 13H), although
Weeksia (Fig. 131), with a prosocline lip, is an
exception. The trochacean lip is usually
prosocline.

Euomphalacean protoconchs were de-
scribed by Yochelson (1956: 195) as “com-
monly discoidal,” but to my knowledge have
not been illustrated. Dzik (1978) illustrated
protoconchs of some Ordovician gastropods
that resemble those of modern archaeo-
gastropods. However, it is not certain whether
any of those he figured are referable to the
Euomphalacea.

The concept of the “radial aperture” was
introduced by Linsley (1977: 196), defined as
“ап aperture whose plane passes through the
axis of coiling and thus lies along a radius
from the coiling axis to the shell periphery.”

McLEAN

Radial apertures are characteristic of all
families in the Euomphalacea. Apertures in
the Trochacea tend to be oblique, or—in
Linsley’s terminology—tangential, defined as
“ап aperture whose plane is tangent to the
body whorl,” so that it and the ventralmost
part of the body whorl lie in one plane.
Multispiral calcareous opercula are known
in the families Omphalocirridae (Fig. 14) and
Oriostomatidae (Figs. 13E, F). Other euom-
phalacean families may have had multispiral
opercula that were uncalcified, or their original
aragonitic opercula may have preserved
poorly compared to the calcitic shell. Such
mineralogic differences between shell and
operculum are known in some Recent tur-
binids and neritids (Adegoke, 1973). The
omphalocirrid operculum is best known in
Liomphalus northi (Fig. 14). It has recently
been described by Yochelson & Linsley
(1972) and Tassell (1976: 9). This type of
operculum varies in thickness, is disc-shaped,
slightly concave externally, beveled to fit tight-
ly within a circular aperture, and has numer-
ous externally visible volutions and internal
laminar layers. It is quite similar to the Cyclo-
spongia operculum, an operculum first
thought to be a sponge, but redetermined by
Solem & Nitecki (1968) as a gastropod oper-
culum from an unknown shell.8 External sur-
faces of opercula are known in two other
omphalocirrids treated by Linsley (1978a).
The oriostomatid operculum is known in
Beraunia (Fig. 13F) (see also Knight, 1941,
pl. 80) and in Oriostoma (Fig. 13E) (see also
Lindstrom, 1884, pl. 17, and Kindle, 1904, pls.
11, 14). Externally, the oriostomatid oper-
culum is conical, in some cases higher than
broad, the central nucleus projecting, the suc-
ceeding whorls descending and having raised
edges. The mode of formation of both the
omphalocirrid and oriostomatid opercula
would be similar, with accretions at the edge
produced in the opercular groove on the ani-
mal’s foot, and adventitious layers added on
the underside, as it rotates in a clockwise di-
rection to produce the counterclockwise coil
of the external surface. These opercula are
unlike the turbinid operculum, in which a

8Yochelson & Linsley (1972) considered that the Cyc/ospongia operculum matches the operculum described by Tyler
(1965: 348, pl. 48, figs. 19-25) and assigned by Tyler to his species Turbinilopsis anacarina. That assignment violates the
well-reasoned hypothesis of Solem & Nitecki that the shell of Cyclospongia must have been a “planorbiform, depressed
helicoidal, or helicoidal shell possessing a circular aperture, deep sutures. . . .” Turbinilopsis as applied by Tyler is assigned
to the Anomphalacea. In my opinion, such a shell is wholly inappropriate for the Cyclospongia operculum because it has a
tangential aperture and lacks an umbilicus. | cannot agree with Yochelson & Linsley (1972) that an operculum as discrete as
those of Liomphalus and Cyclospongia can be convergent in widely different families. | am certain that a euomphalacean
shell eventually will be found for the Cyclospongia operculum.

GALAPAGOS RIFT LIMPET NEOMPHALUS

paucispiral or multispiral pattern is preserved
on the inner surface but is obliterated on the
external surface where it is enveloped by the
animal’s foot. The omphalocirrid and orio-
stomatid opercula differ from the trochid,
turbinid and liotiid opercula in depositing ad-
ventitious layers on the internal surface. Thus,
the euomphalacean and trochacean oper-
cula, though both multispiral, are entirely dif-
ferent. There is convergence in shell form in
the Trochacea and Euomphalacea, but the
distinction may be clearly drawn between
those members in which opercula are known.

Feeding and locomotion: During the pre-
ceding decade a number of papers have con-
sidered possible modes of locomotion and
feeding in the Euomphalacea. The theme has
been developed that these gastropods rested
with the aperture perpendicular to the sub-
stratum, unlike the trochaceans in which
the shell is balanced over the cephalopedal
mass and the aperture maintained in a posi-
tion parallel to the substratum.

Yochelson (1971) discussed open coiling
and septation in the Devonian euomphalid
Nevadispira (which is similar to Serpulospira,
Fig. 13D). He suggested that it had a seden-
tary life mode because an animal with open
coiling would have great difficulty balanc-
ing the shell for locomotion, the septation
that shortened the body mass would further
hamper locomotion, the open coiling would
increase the area of contact with the substrat-
um, and the “hyperstrophic” coiling would
raise the aperture above the sediment. Thus,
this “would appear to be a natural response in
shape change for a coiled animal living a
sedentary life on a mud bottom.” He sug-
gested that euomphalids may have been de-
posit feeders rather than herbivores and that
the open-coiled members “may have further
specialized toward ciliary feeding.” This sug-
gestion was in contrast to the traditional
dictum that all archaeogastropods are herbi-
vorous.

Linsley & Yochelson (1973) discussed
Devonian members of Straparollus (Fig. 13B)
and Euomphalus that had the habit of attach-
ing foreign matter to the shell in a way com-
parable to that of the modern Xenophoridae.
They concluded (1973: 16) that these euom-
phalids were unlikely to have balanced the
shell like trochaceans, it being “most unlikely
that Straparollus laevis could have held its
shell motionless in the normal carrying posi-
tion for the several hours required” for implan-
tation of objects. This was further evidence

317

that euomphalaceans were sessile animals
resting on the base of the shell.

Peel (1975a) also discussed the probability
that open-coiled Paleozoic gastropods were
sedentary. He contrasted open-coiling with
the uncoiling of higher-spired forms, which
also suggests a sedentary existence (see
also Gould, 1969). He concluded that “Paleo-
zoic gastropods were more diverse in their
feeding habits than comparison with extant
gastropods would suggest.”

Linsley (1977, 1978b,. 1978c, 1979) devel-
oped the concept of the radial aperture—in
which the plane of the aperture would pass
through the coiling axis. Gastropods with
radial apertures would have difficulty balanc-
ing the shell over the cephalopedal mass. His
“law of radial apertures” states (1977: 109):
“Gastropods of more than one volution with
radial apertures do not live with the plane of
the aperture parallel to the substrate. Most
typically it is perpendicular to the substrate.”
Few living gastropods have radial apertures.
In one major example, the Architectonicidae,
the animals are mostly sedentary and “usual-
ly lie with the shell on the substrate” (Linsley,
1977). For the Euomphalacea he stated
(1977: 204): “Il suggest that all had adopted a
rather atypical gastropod posture of lying with
the shell flat on the sediment, rarely if ever
hoisting it above the cephalopedal mass in
the stance associated with the majority of
modern forms.” The only possible means of
locomotion would be what Linsley has called
“shell dragging.” In view of the sedentary
habit, Linsley has considered suspension
feeding to be the most likely feeding mode,
“either by filtering with their gill(s) or by cast-
ing mucous nets” (1979: 251).

Schindel (1979) found encrusting epibionts
on the exposed apical cavity surface of the
“hyperstrophic” euomphalid Amphiscapha
(Fig. 13C), whereas the basal surfaces were
free of encrustations. This indicates that the
basal surface was never exposed as would
happen if the life mode involved shell balanc-
ing. This provides further confirmation for
Linsley’s principle.

| can here add the observation that the
oriostomatid operculum precludes locomotion
by shell balancing in that group. Shell-balanc-
ing gastropods use the operculum as a pro-
tective pad placed between the shell and the
foot. In the turbinids the dorsal surface of the
foot envelops the external surface of the
operculum, keeping it smooth, or in some
species producing intricate sculpture. The

318

turbinid operculum is not so thick that it сап-
not be carried in the usual position between
the foot and the shell. However, the conical
oriostomatid operculum, which may be higher
than broad (Fig. 13E), was not enveloped by
the foot (which would have altered its sharp
sculpture) and is too large and sharply point-
ed in the center to have been carried between
the foot and the shell during locomotion.

Extinctions: Euomphalacean genera and
species proliferated in the Paleozoic. Few
stocks survived the mass extinctions at the
close of the Permian. Vermeij (1975, 1977)
correlated their further decline in the Meso-
zoic with the appearance of such shell-crush-
ing predators as teleosts, stomatopods and
decapod crustaceans. The broadly umbilicate
or openly coiled euomphalacean shells are
poorly constructed to resist crushing. There
are few broadly umbilicate forms among
modern marine gastropods. Shells tend to be
sturdier, with narrower apertures, often hav-
ing such modification as apertural dentition or
spiny external surfaces to strengthen the
shell.

More recently Thayer (1979) has discussed
a trend in the evolution of marine benthic
communities. Paleozoic communities on soft
sediments were dominated by immobile sus-
pension feeders such as articulate brachio-
pods, dendroid graptolites, tabulate and
rugose corals, bryozoa, cystoids, and blas-
toids. In the Mesozoic and Cenozoic, the
soft-bottom benthic communities are domi-
nated by infaunal deposit feeders that include
protobranch bivalves, irregular echinoids,
certain crustaceans, holothurians, and an-
nelids. The disruption or bioturbation of the
sediments by the large infaunal deposit feed-
ers would foul or bury the soft-substrate sus-
pension feeders, particularly their juvenile
stages. This, in addition to their vulnerability
to shell-crushing predators, could also ac-
count for the demise of the soft-substrate liv-
ing Euomphalacea, a group not mentioned by
Thayer.

Previous interpretations of euomphalacean
anatomy: The Euomphalacea have been
variously interpreted as either dibranchiate or
unibranchiate. Knight (1952: 40), in his classic
paper on primitive gastropods concluded that
in “hyperstrophic” forms there was “very little
room for a right ctenidium” and assumed that
it and the associated organs had been lost.
Yochelson (1956: 195) considered that the
Euomphalacea were dibranchiate: “The char-
acteristic keel on the upper whorl surface

McLEAN

probably was the locus of an anus as in the
Macluritacea, and the distance of this keel
from the suture would have allowed ample
space in the mantle cavity for paired ctenidia.”
Cox & Knight (1960: 262) took a position on
middle ground: “Right ctenidium inferred to
have been reduced and in some forms pos-
sibly absent.” Golikov & Starobogatov (1975)
included the “Order Macluritida” among the
dibranchiate gastropods.

Linsley (1978c: 440) suggested that
Macluritacea and Euomphalacea “had only
one inhalant and one exhalant stream and
probably only a single gill,’ and that the shape
of the aperture “makes sense if these forms
did not undergo torsion.” Thus, they “there-
fore should not be considered gastropods.”
Linsley’s theory has not as yet been fully de-
tailed. It seems to me, however, that the
euomphalacean operculum strongly suggests
gastropod affinities.

Yochelson (manuscript) now advocates the
removal of genera with a slit from the Euom-
phalacea and finds no indication of an ex-
halant canal in those that remain; he therefore
finds no evidence of paired gills.

My theory for the anatomical reconstruction
of the Euomphalacea includes torsion, allows
both orthostrophy and “hyperstrophy,” and
reconstructs them as unibranchiate, as
Originally proposed by Knight (1952). Peel
(1975a: 218) understood that bipectinate
ctenidia modified for filter feeding would entail
some essential differences from the ctenidia
of modern filter feeders: “The effects of this
difference in the structure or even number of
ctenidia upon the form of a mantle cavity
adapted to ciliary feeding are perhaps impos-
sible to estimate. It is certainly possible that
another arrangement of ctenidia and mantle
cavity was required and that this was at vari-
ance with the elongate ctenidium and long
narrow mantle cavity of the Recent species.”
The neomphalid mantle cavity now provides
the best model for the reconstruction of the
euomphalacean mantle cavity. There is little
essential difference between the filter-feed-
ing mantle cavities of calyptraeid limpets and
the coiled turritellids. The placement of the
neomphalid feeding mechanism within the
eumphalacean shell is equally plausible. |
therefore accept the filter-feeding mode of life
for the euomphalaceans recently suggested
by Yochelson, Peel, and Linsley.

Apart from the ease with which the
neomphalid mantle cavity could be construed
as having been possible within a coiled shell,

GALAPAGOS RIFT LIMPET NEOMPHALUS 319

there is a strong correlation between the
musculature and ontogenetic development of
the shell in Neomphalus and that of the
euomphalaceans, as discussed in the section
that follows.

Neomphalus as a Euomphalacean Derivative

Evidence has been presented in the pre-
ceding section that their radial apertures pre-
cluded the euomphalaceans from balancing
the shell over the cephalopedal mass. Thus
they had to rest the shell on its base, which
was concave for orthostrophic shells or flat for
“hyperstrophic” shells. This is in complete
contrast to the life mode of the trochaceans.

Trochaceans have tangential apertures—
the tangential aperture exposes less body
surface than the radial aperture when the ani-
mal is attached to a hard substratum. The
shell is balanced over the cephalopedal mass
and the columellar muscle is ventral to it dur-
ing locomotion. Even when retracted within
the shell, the cephalopedal mass remains
dorsal to the columellar muscle, which means
that the animal actually rests upon its left side
when the shell is resting upon the base. Thus
the head always maintains a position that is
perpendicular to the axis of coiling. When the
animal extends, a twist in the alignment of the
head of approximately 45° is necessary to
balance the shell, tilting the spire up and to
the right rear.

What can be said about the position of the
head relative to the axis of coiling in the ex-
tinct euomphalaceans? In the absence of shell
balancing, there is no reason to assume that
the cephalopedal mass of mature animals
was aligned to the coiling axis. In normal feed-
ing posture the head of any animal needs to
be balanced relative to the substratum. If the
head and body of a euomphalacean animal in
retracted condition was aligned toward the
coiling axis, a 90° twist would be required to
place it in a feeding posture, an unnecessary
requirement for an animal that never needs to
balance its shell. Moreover, the feeding pos-
ture of a filter-feeding gastropod is one in
which the head remains within the shell aper-
ture, as in Turritella. Most likely the head
would be permanently aligned relative to the
substratum. The columellar muscle would
therefore be lateral rather than ventral to the
cephalopedal mass. Modern gastropods
with irregular coiling have abandoned coiling
and thereby dissociated the columellar mus-
cle from the axis of coiling. For the Euom-

phalacea, my supposition is that regular coil-
ing continues, but the alignment of the body
relative to the coiling axis shifts by 90°. Me-
chanical considerations require that the major
area for muscular insertion on any discoidal
shell be on the inner, columellar wall. Muscle
attachment on any other surface would be un-
necessary. For an animal oriented to the sub-
stratum in a flat-lying shell, this will mean that
the right side of the body assumes the entire
muscle attachment function. There is no need
for a left columellar muscle. The left side of
the body is therefore available for a long,
deep mantle cavity.

Neomphalus is the logical result of the con-
version of the euomphalacean body plan to
the limpet form. One of the most significant
features of Neomphalus is the occlusion by
columellar muscle of the entire right side of
the body posterior to the neck. The columellar
muscle is lateral to the body mass, just as it
must have been in a euomphalacean.

Veliger stages of all gastropod larvae are
similar in having the shell balanced over the
cephalopedal mass. Post-veliger euom-
phalaceans would be motile, would balance
the shell, and would feed by grazing. Growth
of the columellar muscle would Бе рго-
grammed to shift the muscle to the right of the
cephalopedal mass, causing the animal to
lose the shell-balancing capacity and assume
the filter-feeding mode.

In its protoconch and first postprotoconch
whorl, the neomphalid animal must carry its
shell with the coiling axis and plane of the
aperture parallel to the substratum. Its trans-
formation to the limpet form involves cessa-
tion of coiling and a 90° shift of the shell to
place the coiling axis perpendicular to the
substratum. The same 90° shift in the place-
ment of the coiling axis is presumed to occur
in the ontogeny of all the extinct euomphala-
ceans in which the regular coiling continues.
The euomphalacean alters the orientation of
the animal within the shell; the neomphala-
cean effects the change by growth stoppage
along the columellar lip; in both cases the ini-
tial coiling axis becomes perpendicular to the
substratum. This is the essential requirement
in euomphalacean and neomphalacean on-
togeny that distinguishes these superfamilies
from all other living archaeogastropods,
whether coiled or limpet derivatives of coiled
forms.

The relatively large size of the neomphalid
larval operculum and its vestigial retention in
juvenile sizes far larger than that of other

320 McLEAN

limpets is additional evidence that a coiled
ancestry is phylogenetically close. The pres-
ence of epipodial tentacles only near the site
of the operculum is consistent with the idea
that euomphalaceans were filter feeders in
which the head and foot were kept within the
shell in feeding position. There would be no
use of epipodial structures away from the
operculum in euomphalaceans.

The origin of Neomphalus may have been a
rapid event brought about by a relatively sim-
ple alteration of the developmental process,
one that inhibited growth along the basal por-
tion of the columellar lip, forcing continued
growth to produce lip expansion and the for-
mation of a limpet in much the same process
as revealed in the ontogeny of Neomphalus. If
such an event in an euomphalacean stock
took place near an active rift-vent site, the
new limpet would be especially adapted to
utilize the abundant sulphur bacteria in this
rocky environment. Neomphalus represents a
highly successful response to an abundant
food supply, entailing no loss of body size,
using less calcium than that required by a
coiled shell, and affording some protection
from shell-crushing predators. The limpet
conversion represented by the Neomphalidae
was perhaps the only as yet untested
morphological theme in а stock already
specialized for filter feeding.

The Mesozoic euomphalacean family
Weeksiidae, proposed by Sohl (1960), has
some features in common with Neomphalus.
Characters shared by Neomphalus and the
Cretaceous Weeksia (Fig. 131) mentioned by
Sohl (1960: 50) are: “ornament usually poorly
developed . . . growth lines prosocline on up-
per surface... moderately large shell with
raised naticoid protoconch.” The discoidal
shell of Weeksia has an orthostrophic proto-
conch whereas the later whorls are faintly
“hyperstrophic.” The early shell ontogeny of
Neomphalus does not include a stage having
the biangulate lateral profile of weeksiid
genera. However, | have examined speci-
mens of the similarly constructed biangulate
euomphalacen Amphiscapha and note that
the earliest whorls are unsculptured. Thus the
postprotoconch whorls of Weeksia and
Neomphalus can be considered far less dif-
ferent than the mature teleoconch whorls. If
the juvenile shells are to provide the only
characters in common, it is unlikely that the
direct ancestor of Neomphalus will ever be
known.

If Neomphalus was derived from weeksiid
euomphalaceans, the minimal age for the
family would be Cretaceous. Because the
euomphalaceans were the dominant uni-
branchiate gastropods in the Permian, it can
be argued, however, that the Paleozoic, when
numerous stocks were present, is the most
likely time of origin of the Neomphalidae.

Entry of Neomphalus into the Rift-Vent
Community

The rift-vent habitat has probably been
available over long periods of geologic time,
because it is likely that hydrothermal vents
have accompanied tectonic movements
throughout the entire history of the earth. The
oceanic rift system is global in magnitude
(Corliss et al., 1979: 108), although the full
extent of hydrothermal activity along it is un-
known. Vents have not yet been found along
the mid-Atlantic Rift, but at least two widely
separated sites in the Pacific are now known.

As stated by Spiess et al. (1980: 1424):
“The similarity of the East Pacific Rise and
Galapagos Rift fauna suggests that these
vent communities are widespread and that
their species are equipped with sophisticated
dispersal mechanisms well suited for the de-
tection of the discontinuous and ephemeral
vent conditions.” This similarity also suggests
stability of the community. Invasions of spe-
cies from other habitats must be of rather in-
frequent occurrence. Possible barriers to new
colonizations of the community include the
differing chemical conditions, cold water
masses separating the warm environment of
the habitat from other warm environments,
and the scarcity of hard substrates to serve as
stepping stones from shallow water into a
deep-sea hard-substrate environment. Mol-
luscan predators such as sea stars and drill
snails are not known to be present. In the
absence of these predators, the rift-vent com-
munity seems well suited to provide refuge for
an archaic molluscan group specialized for
filter feeding.

Modern filter-feeding gastropods, the tur-
ritellids and the calyptraeids, occur in shallow
water from the intertidal zone to the con-
tinental shelf, with none known from conti-
nental slope or abyssal depths. This evidently
reflects a scarcity of sufficient suspended food
for these relatively large forms under normal
conditions at abyssal depths. A filter-feeding
gastropod the size of Neomphalus would

GALAPAGOS RIFT LIMPET NEOMPHALUS 321

have to have a shallow-water origin, from
which it would make the transition to the rift-
vent community with no interruption in abun-
dance of the food source, through rift-vent
sites in progressively deeper water. A shal-
low-water origin for the Neomphalidae is also
consistent with findings by Clarke (1962) that
no molluscan families have originated in the
deep sea. Shallow water occurrences at one
time are known for all deep-sea mollusks with
continuous Paleozoic to Recent fossil rec-
ords.

There is precedence for the interpretation
of a rift-vent community member as a relict
species. Newman (1979) considered the
stalked barnacle Neolepas zevinae, which he
named from hydrothermal vents on the East
Pacific Rise at 21° N latitude (see Grassle et
al., 1979; Spiess et al., 1980), to represent a
stage of barnacle evolution attained in the
Mesozoic.

Newman’s hypothesis for the origin of
Neolepas is as follows (Newman, 1979: 153):
“Habitat also favors the interpretation that
Neolepas is a relict form, having found refuge
near deep, hydrothermal springs. Such a
refuge may have been attained in the late
Mesozoic when predation pressures on ses-
sile organisms are inferred to have dramatic-
ally increased. Though immigration into the
hydrothermal environment by deep-sea
stocks is a distinct possibility, in the present
case, the route appears more likely to have
been from relatively shallow waters of warm
and tropical seas where tectonically active
rifts intersect continental crust, and perhaps
where islands are forming along ridge crests.”

This explanation provides for both the
antiquity and the route into the rift-vent com-
munity for Neolepas zevinae. It is also the
best hypothesis to account for the presence of
Neomphalus in the rift-vent community. If the
origin of Neomphalus was quickly followed by
submergence, as postulated by Newman for
Neolepas, a fossil record of Neomphalus in
shallow water would be elusory. Fossil rec-
ords of deep-sea mollusks are all but un-
known because of the solubility of calcium
carbonate shells at abyssal depths (Berger,
1978; Killingley et al.,1980).

According to my supposition, the origin of
the Neomphalidae took place at some point
between Late Paleozoic to Late Mesozoic,
giving it an age in the range of 70 to 250
million years. If a fossil record for the family
could verify such an age, it could be called a

“living fossil,” a term limited by Eldredge
(1975) and Stanley (1979: 258) to “taxa that
have persisted for long intervals of time with
little evolutionary change and that are primi-
tive or archaic in comparison with living taxa
of the same class or phylum.” It can be
argued that the neomphalid gill can only be
archaic, since it is not represented in any
other family in normal marine habitats.

If there were a fossil record of the family,
the Neomphalidae could be compared to the
nautiloid cephalopods, the neopilinid mono-
placophorans, the pleurotomariid archaeo-
gastropods, and the abyssochrysid loxone-
mataceans, recently added to the list of living
fossils by Houbrick (1979). These families
were once diverse in shallow seas of the
Paleozoic and Mesozoic but survive now at
the lower limits of the continental shelf to
the abyss. Each family is still represented by
several species. Speciation events have ap-
parently kept pace with extinctions. The aver-
age duration—the Lyellian curve—for marine
gastropod longevity is about 10 million years
(Stanley, 1979: 237). Even if a neomphalid
species could endure as long as 20 or 30 mil-
lion years, numerous speciation events
should have occurred, and other species (or
genera) are likely to be living now at other
rift-vent systems. Ап effective dispersal
mechanism for Neomphalus is unknown. This
is a factor that should increase its speciation
potential, because new colonies would stay
isolated the longer. The possibility that a
single species has represented the family
throughout its entire existence seems the
least plausible alternative.

Reconstruction of Euomphalacean Anatomy

An attempt to reconstruct the anatomy of
euomphalaceans can be based upon two
models: Neomphalus and Turritella. Because
Turritella is a mostly sedentary filter-feeding
animal on soft bottoms (Graham, 1938;
Yonge, 1946), there should be many paral-
lels. Differences between the mesogastropod
Calyptraeidae and the Turritellidae should be
about equivalent to the differences between
Neomphalus and the euomphalaceans.

Coiling differences are reflected in the
orientation of the turritellid and euomphala-
cean mantle cavities. The mantle cavity of the
extremely high-spired Turritella has to turn
like a corkscrew through at least one full
whorl; that of the euomphalacean maintains a

322

horizontal position but has to curve to the
right. It may be a requirement that filament
tips of a bipectinate ctenidium have to relate
to a horizontally aligned food groove; the sin-
gle rack of filaments of a pectinibranch filter-
feeder should have no difficulty relating to the
food groove, whatever the orientation.

Although the columellar muscle of Turritella
is ventral to the cephalopedal mass as in
motile gastropods, the extremely high-spired
shell is too heavy to be balanced for locomo-
tion. In Turritella the early whorls are made
heavy and are partially filled by septation and
deposition of callus (Andrews, 1974). A simi-
lar process of septation and deposition in the
early whorls is also characteristic of euom-
phalacean shells (Yochelson, 1971). Stability
on soft bottoms is thus enhanced in both
groups.

There are remarkable parallels between
Turritella and the euomphalaceans in aper-
ture shape and structure of the operculum. In
both groups the aperture is radial and the
operculum multispiral. The sinuous whorl side
of Turritella marks the position of a dorsal ex-
current siphon; a similar opisthocline sinus in
the upper lip of some euomphalaceans, par-
ticularly the omphalotrochids, can also be in-
terpreted as the excurrent sinus.

In feeding posture Turritella lies partially
buried on soft bottoms so that the operculum
nearly blocks the aperture. The exceptionally
small foot (Yonge, 1946) remains contracted,
sole up, directly behind the operculum (Fretter
& Graham, 1962, figs. 57, 64), except when
used to clear an incurrent depression in the
substratum (Yonge, 1946, fig. 1). Continuous
inhalant and exhalant currents are maintained
unless the foot and operculum are fully re-
tracted.

Placement of the neomphalid anatomy in
the euomphalacean shell would require the
foot to curl forward so that it comes to lie, sole
up, underneath the long neck, which would
position the operculum so that it loosely
blocks the aperture, as in turritellids. In most
euomphalaceans the foot must have been
contained entirely within the aperture, for
there is no ventral gape in the shell. Like the
turritellid foot, the euomphalacean foot would
be relatively small. Because the aperture is so
far to the side of the shell’s center of gravity,
the euomphalaceans were probably no better
adapted for burrowing than for locomotion.

The euomphalacean would have its entire
visceral mass deep within the coils of the
shell. The columellar muscle would be at-

McLEAN

tached about Уз of a whorl behind the aper-
ture and the mantle cavity would extend at
least another third of a whorl deeper. The
neck and head would extend forward of the
area of muscle attachment and would be
broad and flattened as in Neomphalus be-
cause of compression from above and below.
The space above is taken by the free tip to the
ctenidium and the space below is taken by the
foot. A deeply channeled left neck groove like
that of Neomphalus would help to keep some
open space at the left and to provide a rejec-
tion and cleansing channel for the mantle
Cavity.

In Turritella pallial tentacles provide a
coarse filter for the incurrent stream. In
euomphalaceans, tentacles of either pallial or
epipodial origin would be used for that pur-
pose. Other features of the mantle cavity
should be like those of Neomphalus: a bipec-
tinate ctenidium would extend the length of
the mantle cavity, attached ventrally to the
mantle skirt, the free tip emerging near the
region of columellar attachment and extend-
ing over the neck: the split osphradium lo-
cated at the separation of the free tip; the
dorsal afferent membrane lacking, so that the
filament tips from both sides of the gill axis
can reach the food groove; the food groove
extending the full length of the mantle cavity,
running anteriorly over the dorsal surface of
the long neck and cutting directly to the
mouth.

Because both Turritella and the calyptrae-
ids have eyes and anteriorly directed cephalic
tentacles, it is likely that the euomphalacean
head would have such features, having a need
for greater sensory contact outside of the
shell than that of Neomphalus. However, the
dorsal food groove precludes the presence of
a snout, so the most reasonable assumption
is that the head and neck were structured
much like that of Neomphalus.

In Neomphalus a fecal groove extends well
beyond the mid-dorsal anus, the ctenidial fila-
ments keeping the fecal groove in the mantle
skirt well separated from the food groove on
the neck. The same arrangment must have
obtained in the euomphalacean, the general
pattern of water currents in the mantle cavity
being ventral to dorsal, rather than left to right.

The euomphalacean mantle cavity is com-
pletely asymmetrical, extending laterally and
ventrally rather than dorsally over the cephalo-
pedal mass. This asymmetry would also work
to dislodge the primitive juxtaposition of the
rectum and ventricle, so that the complete

GALAPAGOS RIFT LIMPET NEOMPHALUS 323

monotocardian condition is a necessary
consequence of the euomphalacean body
plan. In the absence of a similar leftward dis-
placement of the mantle cavity, the Trochacea
and Neritacea have remained diotocardian,
despite their loss of the right ctenidium.

Although the monotocardian condition is a
likely consequence of the leftward shift of the
mantle cavity, the mesogastropod level of
reproductive advancement need not be. It is
problematic whether these features were pri-
mitive to euomphalaceans or represent an
adaptation of Neomphalus to the rift-vent en-
vironment. It is clear that the genital opening
in euomphalaceans would have to be within
the mantle cavity on the left side. If a copula-
tory-appendage was present, it would have
been on the left side because this is the side
close to the genital opening and there would
be more space for it on the left than the right.
The likely immobility of euomphalaceans
makes it improbable that they could have
moved to copulate effectively. There is no
reason to suggest that broadcast spawning
through an unmodified left kidney would not
be suitable for an immobile animal in concen-
trated shallow-water populations.

If my basic assumption—that the columellar
muscle is positioned to the right rather than
ventral to the body mass of the euomphal-
acean—is valid, then the variable expression
of “hyperstrophy” or orthostrophy can be
considered a result of the shift in position of
the body relative to the columellar muscle.
The direction of coiling then becomes entirely
a matter of convenience to elevate or lower
the aperture above the substratum as an
adaptation to particular bottom conditions.
Thus the hyperstrophy hypothesized for the
Euomphalacea is unlike that of larval archi-
tectonicids or Lanistes in the Ampullariidae, in
which the columellar muscle is always ventral
to the cephalopedal mass. This justifies the
rejection of the term hyperstrophy with refer-
ence to the Euomphalacea.

My theory predicts that ontogeny in a
euomphalacean involves these changes: 1)
the columellar muscle shifts, relative to the
cephalopedal mass, from the ventral position
in the postveliger to the right lateral position in
the adult, 2) the feeding mode changes from
grazing to filter-feeding, which involves
lengthening of the gill filaments, and a corre-
sponding decrease in the relative size of the
radula. The extent to which these changes
were effected could have varied in different
lineages. An incomplete shift in the position of

the muscle would enable retention of shell-
balancing mobility and could account for
some of the more high-spired euomphal-
aceans with shell shapes that converge upon
those of the Trochacea (some oriostomatids,
some euomphalids, some omphalotrochids).
If the radula retained its early prominence, the
initial grazing capacity would be retained.

The relatively high-spired euomphalaceans
could have behaved like the freshwater
mesogastropod Viviparus. Though quite
capable of normal shell-balancing, locomotion
and rasping with the radula, Viviparus also
employs a filter-feeding stance in which the
shell lies half buried, aperture up, the
operculum partially blocking the aperture
(Cook, 1949; Fretter & Graham, 1978).

The fossil chronology indicates that the
earliest euomphalaceans were low-spired
and discoidal. This suggests that the mono-
tocardian condition with a fully bipectinate
ctenidium was primitive to all euomphal-
aceans. Given this premise, many different
expressions of the basic body plan were pos-
sible.

Origin of the Euomphalacea

Although Knight (1952) did not mention the
Euomphalacea in his classic paper on primi-
tive gastropods, he discussed a derivation of
Macluritacea from the Bellerophontacea. Two
years later, Knight, Batten, and Yochelson
(1954) diagrammed a phylogeny of Gastro-
poda in which the Macluritacea were derived
from the Bellerophontacea and the Euom-
phalacea in turn derived from the Malcurit-
acea, a view also followed by Knight et al.
(1960).

Yochelson (manuscript) has a new theory
that seems more compatible with my recon-
struction for the Euomphalacea. He specu-
lates that they could have been derived in the
Ordovician from a Lecanospira-like pleuroto-
mariacean following the loss of the right
ctenidium in a way comparable to the sepa-
rate derivation of the Trochacea. Lecanospira
(Fig. 15B) had previously been regarded by
Knight et al. (1960) as a macluritid, but
Yochelson presents convincing arguments
that it and genera like Lesueurilla (Fig. 15A)
with a deep V-shaped notch in the upper
aperture are best interpreted as pleuroto-
mariaceans. This group of genera was limited
to the early Paleozoic, none being represent-
ed in the extensive euomphalacean fauna of
the Permian (see Yochelson, 1956).

324 McLEAN

FIG. 15. Early Paleozoic genera now excluded from the Euomphalacea for having a prominent raised slit or
selenizone. This group of genera is now regarded (Yochelson manuscript) as the low-spired pleuroto-
mariacean group ancestral to the Euomphalacea. A) Lesueurilla infundibulum (Koken, 1896), Ordovician,
х1.1. В) Lecanospira compacta (Salter, 1859), Ordovician, х1.1. С) Odontomaria elephantina С. F.
Roemer, 1876, Devonian, «0.8. D) Helicotoma planulata Salter, 1859, Ordovician, x 1.6. All after Knight et

al. (1960).

Like euomphalaceans, such genera are
low-spired and discoidal. Open coiling is
represented in Odontomaria (Fig. 15C) (see
also Rohr & Smith, 1978). Lecanospira and
Lesueurilla are “hyperstrophic,” like some
euomphalaceans. This shell form, whether
represented in a unibranchiate or a dibranch-
iate gastropod, presents the same constraints
for locomotion already discussed. Thus these
genera were probably sedentary forms rest-
ing for the most part on their flat bases. As-
suming that they were dibranchiate pleuroto-
mariaceans, the question arises: could these
forms have been filter feeders?

The food groove of Neomphalus provides a
relevant clue, for Neomphalus is the only
known prosobranch in which the food groove
takes a dorsal route to the mouth. In pectini-
branch filter feeders and even in the trochid
Umbonium the right lateral food groove has
developed independently in several families
by “conversion of the tract on the right of
the mantle cavity, along which the food par-
ticles are led to the mouth, into a deep
gutter ... which runs across the whole of the
floor of the mantle cavity to a point just under
the right cephalic tentacle” (Fretter & Graham,
1962: 100). They noted that no living gastro-
pods with paired gills are known to be ciliary
feeders: “The reason for this in zeugobranchs
is most likely to be found in the disposition of
the currents within the mantle cavity—so long
as there are two sets of these, right and left,
converging upon the mid-line, it will prove im-
possible for the material which they carry in

suspension to be collected into a place where
the gastropod may use it. It is only when the
water current is the transverse stream of the
mesogastropod that this happens” (Fretter &
Graham, 1962: 98).

The possibility that the food groove in a
dibranchiate filter-feeder could take a dorsal
route over the head to the mouth has not
heretofore been considered. Lengthened
ctenidial filaments arising from both gills could
converge upon a central food groove. The
food groove of Neomphalus is deflected to-
ward the right before arching toward the
mouth, but this could be a vestige of its primi-
tive mid-dorsal position. Many of the unusual
features of the body plan of Neomphalus can
be understood in terms of additional torsion
and rotation on the anteroposterior axis, as
discussed by Fretter, Graham & McLean
(1981), but no such shifts could account for a
migration of the food groove (or a correspond-
ing ciliated tract) across the right cephalic
complex to a dorsal position. One way to ac-
count for the dorsal position of the food
groove is to consider it a primitive character
shared by the dibranchiate ancestor. Thus
there is good reason to suggest that filter
feeding in a group of low-spired Ordovician
pleurotomariaceans preceded the derivation
of the Euomphalacea.

Diagnosis of the New Suborder Euomphalina

The preceding account of the relationships
between the Euomphalacea and Neomphal-

GALAPAGOS RIFT LIMPET NEOMPHALUS 325

acea is concluded with the proposal of a new
suborder for the two superfamilies, coordinate
in detail with the subordinal definitions of Cox
& Knight (1960) and Knight et al. (1960).

EUOMPHALINA McLean, new suborder

Diagnosis: Shell low-spired to discoidal, or
cap-shaped; coiled shells broadly umbilicate,
aperture radial; operculum (where known)
calcified, multispiral externally, with adventi-
tious layers internally; radula rhipidoglossate;
left ctenidium entirely bipectinate, afferent
membrane lacking; right ctenidium and right
auricle lacking; ventricle not traversed by
rectum; columellar muscle lateral to cephalo-
pedal mass.

The subordinal classification of archaeo-
gastropods in the Treatise (Knight et al.,
1960) has been both inflated (Golikov &
Starobogatov, 1975) and deflated (Salvini-
Plawen, 1980).9

| prefer to follow a middle ground, more or
less equivalent to that of Cox & Knight, recog-
nizing for now three suborders of living uni-
branchiate rhipidoglossates: Euomphalina,
Trochina, and Neritina, each of which has
undergone major radiations that exploited the
evolutionary potential of their very different
body plans.10

The addition of Neomphalus to the ranks of
molluscan classification is a major milestone
in malacology. New finds with as much to con-
tribute to our knowledge of molluscan diversi-
ty and evolution are unusual events. Not since
the discovery of Neopilina has there been
an animal that could fuel so many lines of
speculation. Few living malacologists have
been as privileged as | in having free rein over

such an exciting find.11 Now it is to be hoped
that Neomphalus, like Neopilina, will inspire
others to offer alternative or modified interpre-
tations. One cannot approach the subject of
phylogeny without some preconceived no-
tions, and | could hardly expect that all of
those expressed here will endure.

ACKNOWLEDGMENTS

| am grateful most of all for the opportunity
to report upon this remarkable animal, and |
thank those members of the committee who
offered it to me.

Dr. J. B. Corliss of Oregon State University
preserved the initial collection and forwarded
the material to me. Additional specimens
were sent by Dr. J. F. Grassle of Woods Hole
Oceanographic Institution, Dr. M. L. Jones of
the U.S. National Museum of Natural History,
Dr. R. D. Turner of Harvard University, and
Ms. L. Morse-Porteous of Woods Hole.

Serial sections were expertly prepared by
my volunteer laboratory technician, Jo-Carol
Ramsaran. Superb photograpy of whole and
dissected specimens was done by museum
volunteer Bertram C. Draper. Scanning elec-
tron micrographs of the radula were provided
by Dr. Carole S. Hickman, University of Cali-
fornia, Berkeley (NSF Grant DEB77-14519).
SEM micrographs of the juvenile shells were
made with the assistance of David R. Lind-
berg, University of California, Santa Cruz.

Drafts of the manuscript were read and
helpful commentary offered by Drs. Eugene
V. Coan and A. Myra Keen. Others who may
have read early drafts or have helped in vari-
ous ways through discussion and correspond-

ISalvini-Plawen's (1980: 261) suborder Vetigastropoda for superfamilies “Macluritoidea, Pleurotomarioidea, Cocculinoidea,
Trochoidea, and Murchisonioidea,” “defined by the dominant presence of the (posttorsional) right dorso-ventral retractor
muscle as well as the right excretory organ and bilamellate ctenidia with skeletal rods,” has these difficulties: Neomphalus
with its skeletal rods in the ctenidium lacks the right kidney, and Cocculina has no right kidney, no skeletal rods, nor even a
true ctenidium (Thiele, 1903).

10T 90 little is now known of the Cocculinacea, Lepetellacea and Seguenziacea to include them in this scheme.

11Оуег the three years that | have had Neomphalus under consideration, my conclusions about it have undergone some
major changes. Progress reports have been given at meetings, which occasioned the entry of abstracts in the literature,
some of the statements in which are no longer supported. The first abstract (McLean, 1979) submitted in 1978, drew no firm
conclusion, although | announced at the Geological Society of America meeting in San Jose, California, on 9 April 1979 that |
assigned the limpet to the suborder Macluritina as then understood. On 21 May 1979 | discussed the limpet at the
Symposium on the Biology and Evolution of Mollusca at the Australian Museum, Sydney. The abstract (1980a), which was
completed in April 1979, did not mention the unfound left kidney (so large and thin-walled that is was mistaken for a body
cavity), but it incorrectly stated that the gonads discharge through the right kidney. In 1980 | developed my current view that
the musculature of Neomphalus is the necessary consequence of its ontogeny and phylogeny. On 5 September 1980, for the
Seventh International Malacological Congress in Perpignan, France, my abstract (1980b) incorrectly stated that the left
kidney was vestigial. Fortunately for this novice anatomist, Drs. Fretter and Graham examined the serial section in Septem-
ber, 1980, and agreed to add their expertise to the account of the internal anatomy, resulting in the adjoining paper. The
excretory and reproductive systems proved to be more advanced than | had realized, leaving Neomphalus with fewer of the
archaeogastropod characters than | had originally claimed for it.

326 McLEAN

ence (though not necessarily agreeing with all
of my conclusions) include: R. L. Batten, K. J.
Boss, G. M. Davis, J. F. Grassle, R. R.
Hessler, C. S. Hickman, R. S. Houbrick, M. L.
Jones, D. R. Lindberg, R. M. Linsley, R. A.
Lutz, N. J. Morris, W. A. Newman, J. Pojeta,
Jr., W. F. Ponder, R. Robertson, B. Runnegar,
L. v. Salvini-Plawen, R. S. Scheltema, D. E.
Schindel, and R. D. Turner.

| particularly want to thank my principal re-
viewers, Drs. Vera Fretter of the University of
Reading, England, and Ellis Yochelson of the
U.S. Geological Survey at the National Mu-
seum of Natural History, Washington, D.C.
Vera Fretter has provided helpful review com-
mentary throughout the entire course of this
work. | was especially pleased that she and
Dr. Alastair Graham were able to add their
expertise to the account of the internal
anatomy. My discussion on the Paleozoic
relationships would not have been possible
without the frequent assistance of Ellis
Yochelson, who directed me to many refer-
ences and generously allowed me to cite
some conclusions from his manuscript on the
classification of early gastropods.

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APPENDIX 1: Possible Affinity of
Other Extinct Superfamilies

The search for fossil predecessors to
Neomphalus has led me to consider the rela-
tionships and possible feeding modes of
some other extinct groups. My conclusions
are given in this section.

Shell characters in the Macluritacea and
the Clisospiracea, as in the Euomphalacea,
exceed the limits of diversity now expressed
in the Trochacea. Reasons to dissociate
these two superfamilies from the Euomphal-
acea are given here. The Oriostomatacea
have been synonymized with the Euomphal-
acea in the body of this paper. Reasons to
synonymize the Craspedostomatacea and
Amberleyacea with the Trochacea are given
in Appendix 2. The remaining extinct super-
families recognized by Knight et al. (1960)
and thought to be unibranchiate are the
Pseudophoracea, Platyceratacea, Anom-
phalacea, Microdomatacea, and Palaeotro-
chacea. Commentary on these groups is di-
rected to the question: Do the shell characters
exceed the limits now expressed in the
Trochacea?

MACLURITACEA: The Ordovician genus
Maclurites (Fig. 16A) had an exceptionally
large “hyperstrophic” shell that could only
have rested on its flat base (see Banks &
Johnson, 1957; Knight et al., 1960: 188). A
heavy, protruding operculum fits the aperture.
Internally the operculum has two roughened
areas that have been interpreted as attach-
ment scars for right and left retractor muscles;
externally it is paucispiral with one counter-
clockwise volution, which provides the evi-
dence that led Knight (1952) to interpret its
anatomy as dextral. The Maclurites opercu-
lum is analogous to that of the Neritacea,
upon which left and right columellar muscles
insert, preventing it from rotating to produce a
multispiral pattern. Horn-shaped opercula of a
somewhat different type are known in the
macluritacean genus Teiichispira (Yochelson
& Jones, 1968). The shell of Teiichispira is
poorly known, but Yochelson (1979a: 40) has
concluded that it had a flattened base like that
of Maclurites. Yochelson (in preparation) will
report on the recently discovered operculum
of the macluritid genus Palliseria.

Linsley (1978b, fig. 10) has depicted
Maclurites as a filter-feeding form with the
operculum loosely blocking the aperture in
feeding position. Shells are heavy and the
center of gravity is offset from the aperture.
Linsley has therefore concluded that any

GALAPAGOS RIFT LIMPET NEOMPHALUS 331

FIG. 16. Macluritacea and Clisospiracea. A) Maclurites logani (Salter, 1859), with internal view of opercu-
lum, Ordovician (Macluritacea: Macluritidae), х0.6. В) Onychochilus physa Lindstrom, 1884, Silurian
(Clisospiracea: Onychochilidae), x8.4. С) Mimospira cochleata (Lindstrôm, 1884), basal and apertural
views, Silurian (Clisospiracea: Clisospiridae), x3.4. A & В after Knight et al. (1960), С after Wangberg-

Eriksson (1979).

locomotion was by shell dragging. Maclurites
may have had the pallial configuration of
Neomphalus, but the paired musculature that
has been assumed would entail some major
differences from the Euomphalacea. As noted
earlier, Linsley (1978c: 440) has a theory, not
as yet fully detailed, that the Macluritacea (in
addition to the Euomphalacea) were untorted
and not gastropods. Yochelson (1979b: 347)
has mentioned the possibility that the small
Cambrian Pelagiella could be ancestral to the
Macluritacea, though he now (manuscript)
favors retention of Macluritacea as a gastro-
pod lineage apart from Euomphalacea, rather
than their predecessors, as implied by Knight
et al. (1960).

The Macluritidae are now limited to genera
with horn-shaped opercula; these genera are
known only from the Ordovician. Omphalocir-
rus was transferred to the Euomphalacea by
Yochelson (1966) and Lecanospira (Fig. 15B)
to the Pleurotomariacea (Yochelson manu-
script). The Ordovician Ceratopea is another
genus with a horn-shaped operculum of yet
another kind. Its poorly known shell was first
associated with its well-known operculum by
Yochelson & Wise (1972). The shell is
orthostrophic, thereby differing from other
macluritids, but | would be more inclined to

place it in a family within the Macluritacea
because of its horn-shaped operculum, than
to relate it (as suggested by Yochelson &
Wise) to the suborder Pleurotomariina. In liv-
ing pleurotomariaceans (families Pleuroto-
mariidae and Scissurellidae), the operculum
is multispiral. Wenz (1938: 211) placed
Ceratopea in Macluritidae.

The family Onychochilidae, included by
Knight et al. (1960) in the Macluritacea, is
here transferred to the Clisospiracea, as dis-
cussed under the following heading.

CLISOSPIRACEA: The Clisospiridae (Fig.
16C) and Onychochilidae (Fig. 16B), both
moderately to extremely high-spired and ap-
parently sinistral, are here united in the super-
family Clisospiracea. Although Knight (1952)
included Clisospira among the supposedly
hyperstrophic genera related to Maclurites,
this position was reversed by Knight et al.
(1960), who interpreted Clisospira as sinistral.
The Clisospiracea, then containing only
Clisospiridae, were grouped among those
superfamilies of “doubtful subordinal posi-
tion.” The Onychochilidae were regarded as
dextral-hyperstrophic and were included in
the Macluritacea, apparently in the belief that
there were transitional forms leading to
Maclurites. More recently, Horny (1964), Peel

332 McLEAN

(1975b), and Wangberg-Erikkson (1979)
have found transitional forms between the
Onychochilidae and the Clisospiridae. This
led again to the assumption that clisospirids
were hyperstrophic like the onychochilids and
therefore to the assignment of both families to
the Macluritacea. However, because opercula
are unknown in both families, there is no di-
rect evidence of hyperstrophy, and the entire
assumption is open to question.

Whether the two families were sinistral or
dextral-hyperstrophic, they differ from
Macluritacea and Euomphalacea in having
tangential rather than radial apertures.
Onychochilids and clisospirids would have
been able to clamp to the substratum and
some should have been capable of more ef-
fective locomotion than that of a “shell drag-
ger.” The ontogenetic change in orientation,
which would be required in euomphalacean
and macluritacean development, was not a
component in onychochilid and clisospirid de-
velopment. The tangential rather than radial
aperture plus the lack of the appropriate
opercula is sufficient reason to exclude them
from either the Macluritacea or Euomphal-
acea.

The Clisospiridae, exemplified by Mimo-
spira (Fig. 16C), have moderately high-spired
shells with smooth, concave bases. The only
possible interpretation of the relation of such a
shell to the substratum is that it attached,
limpet-like, to hard surfaces. Hyperstrophy by
definition means that the internal anatomy is
dextral, with water currents flowing left to
right, despite the sinistrality of the shell.
Dextral anatomy is entirely possible within a
high-spired sinistrally coiled shell like the
ampullariid Lanistes (see Cox, 1960: 110, fig.
67), in which the plane of the aperture is near-
ly parallel to the axis of coiling, but it is not
possible in a shell form in which the axis of
coiling is perpendicular to the plane of the
aperture (Fig. 16C). The left ctenidium under
such an impossible condition would be forced
to curve backwards around the columella.
Thus the Clisospiridae could only have been
sinistral in both shell and anatomy. If there is a
transition between the Clisospiridae and the
Onychochilidae, as has been proposed by
Horny, Peel and Wangberg-Erikkson, then it
follows that the Onychochilidae were also
anatomically sinistral. The Devonian Pro-
galerinae (see footnote 3) were regarded by
Knight et al. (1960) as dextral clisospirids. It is
possible that there were dextral as well as
sinistral clisospiraceans, although there are

too few progalerine specimens known to en-
able any firm conclusions.

This analysis, however, is complicated by
the fact that some Mimospira species have
heterostrophic (not hyperstrophic) proto-
conchs (Peel, 1975b: 1528): “The protoconch
is an open-coiled half whorl which, by way of a
perpendicular change in direction of the axis
of coiling from horizontal to vertical, assumes
the hyperstrophic form of the teleconch.” Be-
cause heterostrophic protoconchs are un-
known in Recent archaeogastropods, | offer
no further speculation. Linsley (1977: 204, fig.
7; 1978b: 201, fig. 9; 1978c, figs. 3, 12) has
depicted Onychochilus (Fig. 16B) as carrying
the shell with the spire directed anteriorly over
the head of the animal. Such an unorthodox
interpretation presumably is explained in his
theory (1978c) that the entire group compris-
ing the Macluritacea and Euomphalacea was
untorted. The Onychochilidae appeared in the
Upper Cambrian and thus are among the
earliest known gastropods. A convincing ex-
planation of their form and function would be
of great importance to an understanding of
gastropod phylogeny.

PSEUDOPHORACEA: Linsley et al. (1978)
have discussed the life habits of pseudo-
phorid genera (Fig. 17A) that have a periph-
eral frill, an extension of the base of the shell
serving to raise the position of the aperture
above the substratum. As in the Euomphal-
acea the coiling axis is perpendicular to the
substratum, but the lip growth is prosocline
and the aperture is tangential, so that the
base of the shell is shielded on all sides. They
concluded that the frill-bearing pseudophorids
could have lived on a firm, but not hard, sub-
stratum, much as in the extant deposit-feed-
ing Xenophoridae. Retention of spiral sculp-
ture on the base of the Permian Sallya (Fig.
17A) precludes the limpet-like mode of the liv-
ing calyptraeid Trochita, in which the entire
base of the shell is smooth. The absence of
inhalant access in the shell is no hindrance to
filter-feeding limpets on hard substrates, but
the example of Turritella, as well as that
hypothesized for the Euomphalacea, sug-
gests that filter feeders on soft substrates
would not provide a tentlike shield over the
head. | therefore think that the best hypothe-
sis is that pseudophorids were deposit feed-
ers. Although there are no living trochaceans
with a peripheral frill, there are deposit-feed-
ing trochaceans. | can think of no argument
that would preclude the Pseudophoracea
from having the trochacean pallial complex.

GALAPAGOS RIFT ИМРЕТ NEOMPHALUS 333

FIG. 17. Representative genera of extinct superfamilies discussed in Appendix 1, suborder Trochina. A)
Sallya linsa Yochelson, 1956, Permian (Pseudophoracea: Pseudophoridae), x3.4. В) Platyceras vetustum
J. С. Sowerby, 1829, Mississippian (Platyceratacea: Platyceratidae), х0.6. С) Holopea symmetrica Hall,
1847, Ordovician (Platyceratacea: Holopeidae), х2.3. D) Anomphalus rotulus Meek & Worthen, 1867,
Carboniferous (Anomphalacea: Anomphalidae), х8.4. Е) Microdoma conicum Meek & Worthen, 1867,
Carboniferous (Microdomatacea: Microdomatidae), x 5.7. Е) Palaeotrochus kearneyi (Hall, 1861), Devonian
(Palaeotrochacea: Palaeotrochidae), х0.6. All after Knight et al. (1960).

PLATYCERATACEA: The Platyceratid
limpets (Fig. 17B) have long been understood
to have been coprophagous on crinoids and
cystoids (Bowsher, 1955). Their presumed
coiled predecessors, the Holopeidae (Fig.
17C), had an ordinary trochiform appearance.

Platyceratid limpets had а horseshoe-
shaped muscle scar (see Yochelson, 1956,
pl. 23, figs. 25, 30); the right columellar mus-
cle of Platyceras was evidently large enough
to envelop the mantle cavity as well as the
visceral mass. This provides the argument
that serves to eliminate the group as a possi-
ble predecessor for Neomphalus. The con-
figuration of the platyceratid muscle scar sug-
gests that their derivation as limpets was
parallel to that of the trochid family Stomatel-
lidae, in which the single right columellar
muscle is stretched along the columella as the
whorl expands. There is no evidence to pre-
clude the Platyceratacea from having a man-
tle cavity like that of the Trochacea.

Yochelson & Linsley (1972) described a
calcareous operculum for the Devonian
“Cyclonema” lilydalensis Etheridge, 1891.
They noted that the platyceratid genus

Cyclonema was inappropriate for this spe-
cies, a problem treated recently by Tassell
(1980), who proposed for it the genus Aus-
tralonema in the Holopeidae. Of most interest
here is the fact that the holopeid operculum is
unlike any now known in the Trochacea. This
provides the most useful argument to justify
the retention of Platyceratacea as a super-
family separate from Trochacea.

ANOMPHALACEA: The smooth, mostly
non-umbilicate shells of the Anomphalacea
(Fig. 17D) are streamlined like those of the
Naticidae and Umbonium. They could have
been partially or completely enveloped by the
mantle to enable burrowing in sand. There
are no clues as to feeding habits; probably
they were deposit feeders although the filter
feeding of Umbonium cannot be ruled out.
Nothing precludes their having the troch-
acean mantle cavity.

MICRODOMATACEA: | find no argument
to preclude this small-shelled nacreous group
with tangential apertures (Fig. 17E) from hav-
ing a mantle complex like that of the Troch-
acea.

PALAEOTROCHACEA: Again there is no

334 McLEAN

argument to preclude a mantle complex like
that of the Trochacea in this large-shelled
group (Fig. 17F) with tangential apertures. A
nacreous shell interior has not been demon-
strated, but may prove to have been present.

Conclusion: It is entirely possible that the
trochacean pallial complex, which is so uni-
form in the diverse living trochaceans (Risbec,
1939, 1955; Graham, 1965), could have ac-
counted for all extinct single-gilled archaeo-
gastropod superfamilies other than the
Euomphalacea, Macluritacea, and Cliso-
spiracea.

APPENDIX 2: Suppression of Superfamilies
Craspedostomatacea and Amberleyacea

Two superfamilies proposed by the Treatise
authors in 1960, the Craspedostomatacea and
the Amberleyacea, were grouped by the
authors with other superfamilies of “doubtful
subordinal position.” Evidence for the synony-
mization of these categories with the Troch-
acea is presented as follows:

CRASPEDOSTOMATACEA: This was pro-
posed (Knight et al., 1960: 298) as a “prob-
ably polyphyletic and artificial group,” mostly
having in common the “expanded apertures
in gerontic stages.” Three families were in-
cluded: the Craspedostomatidae, Upper
Ordovician to Silurian; the Codonocheilidae,
Upper Silurian to Middle Jurassic; and the
Crossostomatidae, Middle Triassic to Middle
Jurassic.

Expanded apertures are diagnostic for one
living family in the Trochacea, the Liotiidae. In
addition to the expanded aperture, which is
more of a varix than a completely flared aper-
ture, the family Liotiidae may be recognized
by its flat spire in at least the early whorls, and
predominating axial sculpture of spaced
major ribs and sharp lamellar increments. The
final lip is usually preceded by descent of the
suture, making the aperture more oblique
than that of early stages, in which the aperture
is more nearly radial.12 The Liotiidae can be
traced to the Permian in the genera Dicho-
Заза (Fig. 18A) and Brochidium (see

Yochelson, 1956: 207, 257, and Batten, 1979:
110). These genera have the characteristic
sculpture of liotiids, and are hereby trans-
ferred to the Liotiidae, which places the origin
of the Liotiidae as early as the Permian.

Craspedostoma (Fig. 18C) lacks the spaced
axial ribs of the Liotiidae but has a similar kind
of imbricate sculpture that suggests a suffi-
ciently close relationship with the Liotiidae to
warrant placement of the family Craspedo-
stomatidae in the Trochacea.

In first proposing Craspedostoma, Lind-
strom (1884: 182) remarked: “| have placed
this genus with the Turbinidae in conse-
quence of the congruence of its shell with
several of the Liotidae [sic].” Cossmann
(1918) continued the close association of
Liotiidae and Craspedostoma in adjacent
families. Wenz (1938) separated the two fami-
lies, placing the Craspedostomatidae in the
Trochonematacea and the Liotiinae as a sub-
family of Turbinidae. This led to further sepa-
ration in the raising of Craspedostomatidae to
the superfamily Craspedostomatacea т
Knight et al. (1960), leaving it to the students
of this day to rediscover the affinity between
Craspedostoma and the Liotiidae.

A thickened final lip is present also in the
living trochid genus Danilia (Fig. 18D; see
also Beu & Climo, 1974: 315), as well as in
some small homalopomatine turbinids and
some skeneids. Thus, a thickened final lip is a
recurring theme in the Trochacea. The two
Mesozoic genera in Cox’s family Crosso-
stomatidae may easily be encompassed with-
in the Trochacea; so also at least for the
Mesozoic genera included within the
Codonocheilidae. Accordingly, | recommend
that the Craspedostomatacea be synony-
mized with Trochacea, and that the troch-
acean pallial complex be considered to have
been well established by the Silurian, the time
of appearance of Craspedostoma.

AMBERLEYACEA: This was proposed by
Cox in Knight et al. (1960: 303) for four fami-
lies thought to have been limited to the Trias-
sic through Oligocene. It was characterized
as “a single new superfamily (that) serves to
bring together a number of genera with obvi-

12The Triassic Anisostoma (Fig. 18B), thought by Koken (1897) and Knight et al. (1960) to be euomphalacean, has the final
lip inflated to match the diameter of all previous whorls of the discoidal shell. Its quadrate shell profile resembles that of the
architectonicid Pseudomalaxis. Anisostoma is so bizarre that its true affinity would remain unknown were it not for /aira
evoluta (Reeve), a liotiid with a quadrangular whorl profile and a completely flat spire. In this species, according to Pilsbry
(1934: 380), “the minute axial thread-lineolation usual in Liotiidae is well developed, but other axial sculpture is reduced to
tuberculation of the four subequidistant carinae—at suture, base, and two at periphery.” This description applies equally well
to Anisostoma. In both Anisostoma and llaira the suture descends on the third whorl, though more abruptly in Anisostoma. In
llaira there is no flaring of the lip, but it may be that mature examples with flared lips are yet unknown. The removal of
Anisostoma from the Euomphalacea limits the euomphalaceans to genera that do not have a final varix.

GALAPAGOS RIFT ИМРЕТ NEOMPHALUS 335

FIG. 18. Trochacean genera mentioned in Appendix 2. A) Dichostasis complex Yochelson, 1956, Permian
(Liotiidae), x5.1. В) Anisostoma suessi (Hôrnes, 1855), Triassic (Liotiidae), x1.7. С) Crespedostoma spinu-
losum Lindström, 1884, Silurian (Craspedostomatidae), x1.7. D) Danilia insperata Beu & Climo, 1974, Recent
Trochidae), x 1.2. Е) Amberleya bathonica Cox & Arkel, 1948, Jurassic (Trochidae: Amberleyinae), x 0.8. Fig.
C after Lindstrom, 1884; Fig. D after Beu & Climo, 1974; others after Knight et al. (1960).

ous similarities.” Unifying features were the
nodose or cancellate sculpture and the re-
semblance to the Littorinacea, presumbly be-
cause of the incomplete peritreme in Amber-
leyidae. Nacre was verified only in the Amber-
leyidae; the shell of the other groups may yet
prove to have been nacreous.

Genera in the Amberleyidae have a striking
resemblance to a group of modern genera
that includes Bathybembix, Cidarina, and
Calliotropis. Bathybembix species look like
the Jurassic Amberleya bathonica Cox &
Arkel (Fig. 18E) and many Jurassic species
assigned to Amberleya by Huddleston (1887-
1896) could readily be grouped in the Recent
Cidarina. No reason can be advanced not to
recognize the Recent taxa as a continuation
of this Mesozoic lineage. This lineage has
been in need of subfamilial recognition in the
Trochidae (Hickman, 1980a: 16, and personal
communication), based upon unifying radula
and sculptural characters. The modern line-

age is hereby assigned to the trochid sub-

family Amberleyinae (reduced from the
Amberleyidae).
Removal of Amberleyidae from the

Amberleyacea leaves three other originally in-
cluded families for consideration—the Platy-
acridae, Cirridae, and Nododelphinulidae.
The Platyacridae were characterized in hav-
ing planispiral early whorls, which led Coss-
mann (1915) and Wenz (1938) to place them
in the Euomphalacea. Mature shells are
trochiform. Because planispiral early whorls
occur in the Liotiidae, | have no hesitation in
considering this group as trochacean. Be-
cause of its discoidal final whorl, the sinistral
Cirrus was thought to be euomphalacean by
Cossmann (1915) and Wenz (1938). How-
ever, it and other genera included in the Cir-
ridae have the spinose sculpture of the
Amberleyinae. | doubt that Cirridae is a natu-
ral group, for few prosobranch families are
completely sinistral. Because of the close re-

336 McLEAN

semblance between Amberleya and Cirrus,
the Cirridae are easily encompassed within
the Trochacea. The five genera of Cox’s
Nododelphinulidae exhibit many sculptural
features of both the Liotiidae and the genus
Angaria; these genera are also easily placed
within the Trochacea.

Conclusions: A comparison of treatments
by Cossmann (1915, 1918), Wenz (1938) and
the Treatise authors (1960), leads me to be-
lieve that taxonomic inflation of supraspecific
categories has obscured some relationships.
The Treatise authors introduced two new
superfamilies with very weak justifications.
They evidently followed Wenz's dogma that
the Trochacea arose in the Triassic; there-
fore, everything occurring in the Paleozoic
had to be placed elsewhere. If Wenz or the
Treatise authors had pursued Lindstrom’s ог
Cossmann’s recognition of an affinity be-
tween Craspedostoma and Liotia, the ac-
cepted classification of today would have

been very different.

The suprageneric classification of the
Trochacea is greatly in need of revision. | sug-
gest that as a prelude to a new understanding
of the Trochacea, the available families and
subfamilies of the currently recognized
Craspedostomatacea and Amberleyacea be
reconsidered as possible familial or subfamil-
ial lineages in the Trochacea. Many of the
Mesozoic genera now uncomfortably left in
the Euomphalacea also need to be recon-
sidered as possible trochaceans. The roots of
the great radiation of the Trochacea are in the
Paleozoic, as evidenced by the clear pres-
ence of the Liotiidae in the Permian and the
likelihood that the Silurian Craspedostoma
was also trochacean. Some members of other
Paleozoic superfamilies also need to be con-
sidered as possible trochaceans, because
few arguments can be advanced to disprove
an affinity with the Trochacea (see Appendix

1).

MALACOLOGIA, 1981, 21(1-2): 337-361

THE ANATOMY OF THE GALAPAGOS RIFT LIMPET, NEOMPHALUS FRETTERAE!

Vera Fretter,2 Alastair Graham? and James H. McLean?

ABSTRACT

Neomphalus fretterae is limpet-shaped, the mantle cavity extending from the right side of the
head anteriorly and along the whole left side of the animal. The ctenidial axis stretches from the
inner end of the cavity to its mouth attached to the mantle skirt, and then freely for a distance
equal to about a fourth of its total length. The filaments are supported by skeletal strips united at
their base to strengthen the axis; they are elongated, lie across the cavity, their tips related to a
ciliated food groove which runs from the posterior end of the cavity to its mouth and thence
forward on the right side of the neck, dorsal to the right tentacle, to the mouth.

The buccal region contains jaws and an odontophore, the musculature of which is described.
The mid-esophagus is elongated, dilated and glandular, but has no septa and shows no torsion.
The posterior esophagus runs alongside the right side of the mantle cavity to a stomach with
gastric shield and vestigial spiral caecum. The intestine has an anterior loop alongside the
esophagus, does not enter the pericardial cavity, and opens by the anus, placed on the anterior
border of the shell muscle.

The heart, consisting of one auricle and a ventricle, lies in a pericardial cavity placed pos-
teriorly and sending prolongations into the visceral mass. Anterior and posterior aortae arise
from a bulbus. The general plan of the circulation is as in monotocardians, with a renal portal
system. All vessels have an endothelial lining. There is one kidney, the left, opening to the
mantle cavity; it is greatly dilated, forms a body cavity round much of the gut and possesses a
nephridial gland. No renopericardial canal was found. The nervous system is hypoathroid-
dystenoid, with long cerebropleuropedal connectives and scalariform pedal cords. Many nerve
cells lie in the nerves. The streptoneury of the visceral loop is very tight. There is a prominent
branchial ganglion, small osphradia lie on the gill axis and a statocyst over each pedal ganglion.
There are no eyes.

The sexes are separate, males normally distinguishable by the greater length of the left
cephalic tentacle. The testis discharges to a large prostate gland opening to the mantle cavity
near the anus; a seminal groove leads along the left side of the neck, whence a ciliated tract runs
along the tentacle. In females the ovary opens to a U-shaped oviduct with two different glandu-
lar areas. A ciliated groove runs along the oviduct and originates at the mouth of a receptaculum
seminis opening separately to the mantle cavity at a deeper level.

The anatomical peculiarities of Neomphalus are mainly brought about by (1) adoption of a
patelliform facies; (2) enlargement of the mantle cavity; (3) an increased torsion (270°) of
visceral mass on head-foot; (4) a leftwards roll of mantle cavity and visceral mass on an
anteroposterior axis. The animal cannot be related to any living group of prosobranchs. It shows
several features—gill, radula, anterior intestinal loop—characteristic of archaeogastropods, but
in most respects the organization is monotocardian, in some ways convergent with that of other
ciliary feeders. Neomphalus seems to represent a prosobranch stock passing from the archaeo-
gastropod to the mesogastropod grade which has persisted by virtue of its unusual habitat.

INTRODUCTION

In the following pages an account is given
of the internal anatomy of Neomphalus fret-
terae, its bearings on the functioning of the
living animal and on its relationships. The ex-
ternal features of the Galapagos Rift limpet
have already been described (McLean, 1981)

and are not dealt with here. The source of the
animals and their mode of preservation have
been given in the same paper. Much informa-
tion was gained from study of serial sections,
sagittal and transverse, cut 15 ит thick and
stained in Mayer's hematoxylin and eosin;
animals were also dissected with the help of a
stereomicroscope.

1Contribution number 29 of the Galapagos Rift Biology Expedition supported by the [United States] National Science

Foundation.

2University of Reading, Whiteknights, Reading RG6 2AJ, United Kingdom.
3Los Angeles County Museum of Natural History, Los Angeles, California, U.S.A. 90007.

(337)

338 FRETTER, GRAHAM AND MCLEAN

ANATOMY
Ctenidium

The ctenidial axis (Fig. 1) consists of a
tough skeleton of connective tissue with a
bundle of longitudinal muscle fibers running
dorsal to the afferent vessel. The efferent
vessel, placed where the axis attaches to the
mantle skirt, is surrounded by a thick wall of
connective tissue strengthened on each side
by the fibrous bases of the skeleton of the
filaments.

The ctenidial filaments are attached ob-
liquely to the axis, the afferent end anterior to
the efferent. Each is flattened but bulges
slightly along the afferent and efferent bor-
ders. The efferent edge is supported by two
dense and fibrous skeletal rods which taper
dorsally and do not extend far towards the
afferent edge throughout the greater part of
the length of the filament. Near its attachment
to the axis, however, the skeletal rods be-
come longer and thicker, extending over more

of the depth of the filament. Finally, near the
axis, neighbouring filaments fuse and the
skeletal rod on the side of one filament joins
with that on the adjacent side of the next fila-
ment; still nearer the axis this unites with cor-
responding pieces in other filaments so that a
zigzag skeletal structure is produced. This lies
in the wall of the efferent vessel. Since there
is a double row of filaments the result is that
the efferent and the sides of the axis are
braced by a complex and continuous skeletal
support.

The narrow efferent edge of the filament
carries some frontal cilia; its afferent edge
carries abfrontals, as numerous as the fron-
tals. The most conspicuous ciliation, however,
is the set of strong lateral cilia placed on each
flat side of the filament. The gill is therefore
clearly equipped with the ciliation necessary
to drive water from the lower, ventral side of
the mantle cavity to the dorsal, and to move
particles filtered from this stream to the tips of
the filaments, where they are deposited in, or
may be led to, the food groove.

MC ms

FIG. 1. Stereogram of part of mantle skirt, a short length of ctenidial axis, and the bases of five filaments on
one side; those on the other side are not shown. The filaments are cut successively closer to the axis from
left to right. Arrow shows direction of water current. ab, afferent branchial vessel in ctenidial axis; ac, ab-
frontal cilia; af, afferent vessel of filament; ct, ctenidial axis; eb, efferent branchial vessel in ctenidial axis; ef,
efferent vessel of filament; fc, frontal cilia; Ic, lateral cilia; mc, mantle cavity; ms, mantle skirt, s, gill skeleton.

ANATOMY OF NEOMPHALUS 339

FIG. 2. Animal in dorsal view to show the general plan of the alimentary canal together with some features of
the mantle cavity and head. a, anus; ai, anterior intestinal loop running above and below posterior esopha-
gus; b, bulbus, dividing anteriorly into anterior and posterior aortae; c, spiral caecum; d, one of the ducts of
the digestive gland (the position of others is indicated and the extent of the gland is stippled); f, food groove;
g, gastric shield; i, innermost part of mantle cavity; L, left; |, oral lappet; m, position of mouth; me, mid-
esophagus; mp, male pore, its lips extending right, ventral to the rectum; ms, mantle skirt, the pecked line
indicating where it has been cut; о, odontophore; р, pericardial cavity; pe, posterior esophagus; В, right; г,
rectum; rs, radular sac; s, salivary gland; sg, seminal groove running on to left tentacle; sm, shell muscle,
hatched; st, stomach; t, tentacle.

340 FRETTER, GRAHAM AND MCLEAN

Digestive system

The mouth (Figs. 2-5), a longitudinal slit
when closed, is placed on the underside of
the head practically at the extreme anterior
end of the body. The short, vertically-directed
oral tube to which it opens carries a jaw on
each lateral wall. These are oval cuticular
thickenings tapering ventrally to a thin edge.
Their surface is smooth.

The buccal cavity is wide and has a well-
developed odontophore on its floor with a
rather shallow sublingual pouch beneath it.
Between the point where the cerebral com-
missure crosses the roof of the cavity and the
beginnings of the dorsal folds of the esopha-
gus the roof is folded outwards to form a glan-
dular pouch on each side of the mid-line:
these may represent salivary glands; other-
wise none are present. Dorsal to the odon-
tophore is an opening leading to a broad but
shallow space, the radular diverticulum; it
rapidly narrows posteriorly and from its in-
nermost part the radular sac runs back.

The esophageal opening lies dorsal to that
of the diverticulum and is slit-like, narrow dor-
soventrally and wide laterally. Behind the
level of the cerebral ganglia, and about level
with the mid-points of the odontophoral carti-
lages, the lateral parts of the esophagus ex-
pand ventrally so that the gut has a deep in-
verted U-shape in section. Dorsally its walls
bear two longitudinal folds, low and well sep-
arated, and ventrally two similar ones. On
each side one dorsal and one ventral fold
separate a lateral pouch from a central area.
Posterior to the tip of the radular sac the
esophagus gradually becomes approximately
circular in section, the ventral folds converge
on the mid-ventral line and unite to form a
single fold with a double free edge. All three
folds run the whole length of this region of the
esophagus, becoming taller posteriorly. They
terminate when the esophagus is close to the
level of the pleuropedal ganglia. Here the la-
teral pouches end, the diameter of the gut is
abruptly reduced—it is tightly embraced by
the visceral loop—and the wall becomes
thrown into many low longitudinal folds, mark-
ing the beginning of the posterior esophagus.
Although this is where one would expect to
see the effects of torsion on the gut there is no
sign of the twist visible in most prosobranchs,
though it is clear in the vascular and nervous
systems.

The posterior esophagus runs back, on the

left side of the body, to the visceral mass
where it curves to the right and runs through
the digestive gland to enter the stomach (Fig.
6). This is a U-shaped structure embedded in
the gland, dorsoventrally flattened, the con-
cavity facing left, with the esophagus entering
the anterior limb and the intestine leaving the
posterior one. Five ducts, all opening to the
esophageal half, connect the stomach and di-
gestive gland. At the apex of the stomach, on
the right, a small, twisted tubular appendage,
its walls bearing some ridges and grooves,
seems to be a vestige of a spiral caecum, and
on the ма! of the intestinal limb lies an oval
cuticular patch, raised marginally into crests,
which must represent the gastric shield of
other prosobranchs. Though much of the
stomach wall is rather featureless, a ciliated
intestinal groove can be recognized running
along the intestinal limb and bordered by
slightly elevated typhlosoles. This part there-
fore corresponds to the style sac of other
prosobranchs.

The intestine passes from the stomach to
the left and loops forward through the kidney,
attached to its wall ventrally; emerging from
this it enters the cephalopedal sinus and
passes anteriorly, ventral to the posterior
esophagus almost to the level of the supra-
esophageal ganglion. There it turns through
180°, curves to the dorsal side of the esoph-
agus and runs back nearly to the level of the
anterior end of the pericardial cavity. Here it
again projects into the kidney, and, skirting
the pericardial cavity turns forward as the rec-
tum, passing close to the efferent renal vein.
Finally, it emerges from the kidney and, after
a short course along the roof of the mantle
cavity, opens by the anus which lies more or
less in the mid-line of the head-foot and on the
anterior edge of the shell muscle (Fig. 11A).

Except for that part which lies anterior to the
posterior esophagus the alimentary tract is
lined everywhere by a columnar ciliated epi-
thelium with numerous goblet cells; additional
gland cells of another type occur in the rec-
tum, presumably concerned with the consoli-
dation of fecal material. The initial part of the
esophagus, however, may be divided into la-
teral unciliated, glandular areas, where the
cells exhibit apocrine secretion, located be-
tween the ciliated dorsal and ventral folds on
each side, and a ciliated channel between the
two dorsal folds. Though the development of
the lateral glandular areas is much less than
in other archaeogastropods—particularly in

ANATOMY OF NEOMPHALUS 341

the absence of folding of the epithelium—it is
distinct, and, despite the fact that it lies an-
terior to the region of torsion instead of coin-
cident with it as in these animals, its organiza-
tion allows this part of the gut to be identified
as mid-esophagus.

In general the gastric epithelium is a simple
ciliated columnar one. That underlying the
gastric shield, however, stains more darkly
and at intervals small protuberances project
from it, away from the stomach lumen. These
consist of bundles of cells, about twice as high
as the ordinary gastric ones. Each bunch is
bound by small muscle fibres. From their situ-
ation it may be presumed that they produce
the cuticular material.

The digestive gland is markedly less volu-

D
5
К

ERS
RT
A

SIE

== ==

minous than in most archaeogastropods. Its
tubules are lined by cells which seem highly
vacuolated and devoid of contents in the ani-
mals examined, staining very lightly. These
correspond to the digestive cells of other pro-
sobranchs. Other cells also appear, reminis-
cent of the glandular cells of these animals,
darkly staining, with a swollen base lying
against the surrounding blood space and
connected to the lumen by a narrow neck.
Sometimes these cells appear to be grouped.
Some of the digestive cells bulge outwards
into the blood spaces lying between tubules.
Occasionally we have gained the impression
that narrow, tubular spaces, lined by darkly-
staining cells, project from the tubules into the
blood spaces; there they turn to run briefly in

UD fr Dim (VW. аа

FIG. 3. Right sagittal half of the head and buccal mass. aa, anterior aorta (cephalic artery) which divides
anteriorly into a dorsally-directed buccal artery and two lateral cerebral arteries; ac, approximator muscle of
the cartilages; bc, buccal commissure running in the transverse fold; bd, buccal dilator muscle; br, buccal
constrictor muscle; cc, cerebral commissure; cg, cerebral ganglion; dj, depressor muscle of the jaw which
posteriorly fuses with muscles from the walls of the sublingual pouch and with the retractor of the radular
membrane; dw, dorsal body wall; e, esophagus; ed, dilator muscles of the esophagus; |, jaw; |, levator
muscle of jaw; ol, levator muscle of the odontophore; prm, protractor of the radular membrane; rd, radular
diverticulum; rj, retractor (remotor) muscle of the jaw; rr, radular retractor muscle; rs, radular sac; rsm,
retractor muscle of the radular membrane; rtf, retractor muscle of the transverse fold; sg, salivary gland; vp,
ventral protractor muscle of the odontophore; vw, ventral body wall.

342 FRETTER, GRAHAM AND McLEAN

the hemocoel, parallel to the base of the epi-
thelium. They would thus seem comparable to
short tubular glands. The fixation of the mate-
rial, however, has not been good enough to
let us resolve these structures clearly. Nu-

merous amebocytes, their cytoplasm contain-
ing yellow granules, occur in the blood
spaces.

The intestine and rectum contain through-
out most of their length a fecal rod, pieces of

FIG. 4. Arrangement of muscles and related structures of the buccal mass; dorsal view. The central black
spot indicates where the buccal artery opens from below into the buccal sinus. aa, anterior aorta (cephalic
artery); ben, buccal connective; bd, buccal dilator muscle; bg, buccal ganglion; br, buccal constrictor muscle;
c, buccal cartilage; cc, cerebral commissure; cg, cerebral ganglion; cp, cerebropleural and cerebropedal
connectives; e, esophagus; j, jaw; m, mouth; ol, odontophoral levator muscle; prd, posterior boundary of the
radular diverticulum; prm, protractor of the radular membrane; rr, radular retractor muscle; rs, radular sac;
rsm, retractor muscle of the radular membrane; rtf, retractor muscle of the transverse fold; to, anterior tip of
odontophore; vp, ventral protractor of the odontophore.

ANATOMY OF NEOMPHALUS 343

which may also be seen within the mantle
cavity. This contains much particulate matter
of varied sorts, mainly minute, but pieces of
grit, radiolarian, foraminiferan and crustacean
skeleton are also numerous and often of con-

siderable size. The largest pieces of crusta-
cean skeleton seen measured about 250 x
90 ит, and the largest piece of radiolarian
skeleton about 200 x 110 ит. The rod is
composed of mucus; in the rectal region and

FIG. 5. Arrangement of muscles and related structures of the buccal mass; ventral view. aa, anterior aorta
(cephalic artery) branching anteriorly into right and left cerebral arteries running to cerebral ganglia, and
buccal artery passing dorsally to buccal sinuses; br, buccal constrictor muscle; c, buccal cartilage; cc,
cerebral commissure; cg, cerebral ganglion; cp, cerebropleural and cerebropedal connectives; dj, depressor
muscle of jaw; e, esophagus; j, jaw; |, levator muscle of jaw; т, mouth; prm, protractor muscle of radular
membrane; psp, posterior limit of sublingual pouch; rj, remotor muscle of jaw, cut where it penetrates the
depressor of the jaw on its way to the ventral body wall; rr, radular retractor muscle; rs, radular sac; rsm,
retractor muscle of the radular membrane; to, anterior tip of the odontophore; tsp, tensor muscles of the
sublingual pouch; vp, ventral protractor muscle of the odontophore.

344

anne ТО

OS pests 1
E 0:2 mm
FIG. 6. The stomach in dorsal view. A, anterior; c,
vestigial spiral caecum; dd, ducts of digestive gland
(the position of others indicated); e, esophagus; gs,
gastric shield; i, intestine; ig, intestinal groove; L,
left; P, posterior; R, right.

mantle cavity it acquires a superficial layer
with the same staining reaction as the rectal
glands and probably derived from them, main-
taining the integrity of the rod until it has
passed out of the cavity.

The buccal region is organized as in other
prosobranchs to allow the use of the odon-
tophore and radula which are supported by a
single pair of cartilages. The muscles associ-
ated with this apparatus are as follows (Figs.
3-5):

A. Muscles from the jaws and buccal roof.

1. Dilators of the buccal cavity (Figs. 3, 4,
bd). Numerous small muscles run from the
dorsal and dorsolateral walls of the oral tube
and anterior part of the buccal cavity to origins
in the body wall anteriorly and dorsally.

2. Levators (or retractors) of the jaws
(Figs. 3, 5, lj). On each side a muscle runs
from an origin in the anterodorsal body wall to
an insertion centrally placed on the ventral
half of the jaw.

3. Depressors and remotors of the jaws.
On each side there are two muscles. The
more powerful, the depressor (Figs. 3, 5, dj),

FRETTER, GRAHAM AND MCLEAN

is inserted centrally on the dorsal region of the
jaw and surrounding buccal wall, whence it
passes ventrally to the mid-line where the
muscles from right and left jaws unite and
there is some decussation of the fibres. Under
the sublingual pouch splits appear in the
muscle allowing fibers of the remotor muscle
of each side to pass medially. Thereafter the
depressors run posteriorly as a single muscle
but bifurcate into right and left portions again
round the buccal artery. Each half then at-
taches to the ventral side of the ipselateral
Cartilage.

The second muscle, the remotor (Figs. 3, 5,
rj), is weaker. It is inserted on the jaw ven-
trally, close to the levator, passes back to lie
ventral to the sublingual pouch, penetrates
the depressor and then fuses with the ventral
musculature of the head.

4. Constrictors of the mouth and buccal
cavity (Figs. 3, 4, 5, br). A band of muscle
Originates on the lateral wall of each cartilage,
more or less centrally. It runs forward ventral
to the lateral expansion of the buccal cavity
and terminates in the mid-line anteriorly
(where it now lies morphologically dorsal to,
but topographically anterior to the gut) partly
by attaching to the buccal wall, partly by in-
termingling with its contralateral partner. In
this way a sling muscle is formed which on
contraction closes the mouth and constricts
the anterior buccal region.

B. Muscles related to the radular membrane.

1. Protractors of the radular membrane
(Figs. 3, 4, 5, prm). A pair of muscles inserts
on the radular membrane where it forms the
roof of the mouth of the sublingual pouch, one
on either side of the mid-line. They run pos-
teriorly to a point alongside the buccal artery
then, one on either side of the vessel, pass
ventrally with it to the inner side of the mus-
culature of the neck. They travel posteriorly
here, one on either side of the cephalic artery,
almost as far as the pleuropedal ganglia,
gradually attenuating as their fibers attach to
body wall muscles. Contraction of these
muscles brings the radular membrane and
teeth outwards over the odontophoral tip.

2. Retractors of the radular membrane
(Figs. 3, 4, 5, rsm). These are well developed
and easily the most powerful components of
the buccal musculature. They originate ven-
trally on each cartilage, some fibers on the
medial side but most ventrolaterally and run
thence dorsally and anteriorly to insertions on

ANATOMY OF NEOMPHALUS 345

the radular membrane. Their action retracts
the membrane and teeth.

3. Radular retractors (Figs. 3, 4, 5, rr). On
each side a muscle is inserted on the most
medial parts of the radular membrane dorsally
and on the side walls of the anterior half of the
radular sac. Posterior to the cartilages these
muscles diverge laterally, pass ventrally and
enter canals in the lateroventral musculature
of the body wall, where they gradually inter-
mingle with the intrinsic muscles. Their action
is synergic with that of the main retractors but
also affects the radular sac.

C. Protractors and levators of the odonto-
phore.

1. Ventral protractors (Figs. 3, 4, 5, vp).
On each side a muscle runs forwards, later-
ally and ventrally from the posteroventral end
of the cartilage. Posterior to the level of the
mouth it passes into a channel penetrating the
body wall musculature amongst the fibres of
which it has its origin.

2. Levators (Figs. 3, 4, ol). A muscle in-
serts on the anterior part of each cartilage
laterally. It passes dorsally, laterally and
somewhat posteriorly, above the cerebral
ganglion, to penetrate the dorsolateral body
wall muscles where its fibers originate. Its ac-
tion retracts and elevates the anterior part of
the odontophore.

D. Other muscles. These are associated with
the sublingual pouch, with the radular diver-
ticulum, and run between the cartilages.

1. Retractors of the transverse fold (Figs.
3, 4, rtf). A small muscle orginates on the pos-
terior end of each cartilage dorsally. It runs
forward and medially giving off a thin sheet
laterally to the medial wall of the esophagus
on the same side. More anteriorly it crosses
the mid-line and ends in the tissue of the
transverse fold (the sheet of tissue between
radular sac, radular diverticulum and esopha-
geal floor, in which the buccal ganglia lie).
Some fibers of each muscle continue on the
ipselateral side and there is a marked cross-
tie between the right and left muscles poste-
rior to the point of decussation.

2. Tensors of the sublingual pouch (Fig.
5, tsp). Small muscles are inserted on each
side on the roof, inner end and floor of the
sublingual pouch. All pass posteriorly, lateral
to the buccal artery and protractors of the
radular membrane, intermingle with the de-

pressor muscle of the jaw and finally originate
on the posterior medioventral region of the
cartilage. Thus when the jaws and odonto-
phore are protruded through the open mouth,
the position of the walls of the sublingual
pouch is adjusted to clear the passage and
allow the radular teeth to move forward and
downward.

3. Approximator of the cartilages (Fig. 3,
ac). This is a prominent muscle which runs
across the mid-line from the median ventral
face of one cartilage to a corresponding situa-
tion on the other. On approximation of the car-
tilages ventrally their dorsal ends diverge, so
spreading the radula.

Circulatory system

The part of the pericardial cavity which con-
tains the heart (Fig. 7) lies left of the mid-line
at the extreme posterior end of the visceral
mass, bordered on the left by the innermost
part of the mantle cavity and on the right by
the posterior end of the shell muscle. It is
somewhat triangular in outline, the longest
side against the mantle cavity, narrow anteri-
orly and posteriorly. From the main cavity two
extensions penetrate the visceral mass, one
arising dorsally and passing forwards be-
tween gonad and digestive gland, lying di-
rectly under the mantle; the second starts
ventrally, close to the bulbus, and runs ante-
riorly, again between gonad (which lies dorsal
to it) and digestive gland (which is ventral to
it). The two extensions meet and fuse ante-
riorly. They are narrow clefts throughout their
course.

In most places the pericardial cavity is lined
by a squamous epithelium. In some areas,
however, the epithelium is columnar, its cells
loaded with spherules staining brightly with
eosin and often giving evidence of apocrine
secretion into the lumen. This type of cell is
restricted to the pericardial wall in the neigh-
borhood of the bulbus and to the extensions
into the visceral mass; in all situations, how-
ever, it occurs only where pericardial wall
abuts against tubules of digestive gland.

There is only one auricle, the left, and there
is no indication of a right one. It has a fusiform
shape and lies partly posterior to and partly
alongside the ventricle, on its left. Its wall is
not markedly muscular and few muscular
strands cross its lumen. Though the wall is
generally smooth externally there are clear
signs of filtration chambers as described in
Viviparus (Andrews, 1979). The auricle com-

346 FRETTER, GRAHAM AND MCLEAN
chamber with much muscle in its wall and
crossing its lumen, on the strands of which sit
cells filled with brown granules. Anteriorly and
ventrally the ventricle narrows to a short,
muscular bulbus which passes out of the peri-

municates more or less at its mid-point with
the ventricle by a small opening, the lip of
which projects a little into the ventricular cav-
ity, acting as a valve in the absence of true
valves. The ventricle is a rather globular

rs
1 mm

ius ast

AA я nenne
LITT a
Lit? +
Pas г x

(MNS

FIG. 7. Semi-diagrammatic representation of the relationships of the vascular, excretory and nervous sys-
tems at the posterior end of the mantle cavity and visceral mass. In life the right and left parts of the visceral
loop (rv and lv) lie more or less vertically over one another: to make the anatomy clearer they have been
spread apart by pushing the left structures over to the right of the figure. A, anterior; a, auricle; aa, anterior
aorta within cephalopedal sinus; ab, afferent branchial vessel (in dorsal part of ctenidial axis); b, bulbus; cs,
cephalopedal sinus; cv, circumpallial vessel; eb, efferent branchial vessel (in ventral part of ctenidial axis); k,
kidney; ko, kidney opening; L, left; lv, left visceral ganglion in floor of kidney; m, limit of mantle cavity; ng,
nephridial gland; P, posterior; p, extension of pericardial cavity into visceral mass; pa, posterior aorta within

venous visceral sinus; pc, main pericardial cavity; pv, pallial vein; R, right; rs, vessel of rectal sinus connect-
ing with plexus in kidney wall; rv, right half of visceral loop about to enter kidney; v, ventricle; vs, visceral

sinus.

ANATOMY OF NEOMPHALUS 347

cardial cavity to lie on the ventral side of the
visceral mass where that is connected to the
head-foot. It rapidly divides into posterior and
anterior aortae.

The posterior aorta passes to the right in a
visceral venous sinus close to the ventral sur-
face of the visceral mass. It sends branches to
the nephridial gland, the kidney, digestive
gland and reproductive organs.

The anterior aorta runs in the cephalopedal
sinus (vein) and passes to the left side of the
head-foot in close proximity to the anterior
loop of the intestine and the posterior esoph-
agus. It soon gives off a large pallial artery
which passes to the floor of the mantle cavity
and is traceable there to the anterior and pos-
terior ends of the animal and is almost cer-
tainly circumpallial. The aorta runs forward to
the level of the pleuropedal ganglia where it
passes, parallel to the supra-esophageal
connective, from a position dorsal to the
esophagus to one ventral to it and gives rise
to right and left lateral pedal arteries. These
pass into the lateral parts of the foot, run
backwards and forwards and give off numer-
ous branches. The aorta (now properly the
cephalic artery) continues forward in the floor
of the cephalic hemocoel between the right
and left protractor muscles of the radular
membrane to a point about midway along the
length of the odontophoral cartilages and just
posterior to the sublingual pouch. Here it
splits into three: (1) the buccal artery, which
passes dorsally and opens to blood sinuses in
the odontophore and round the radular sac;
(2) and (3) lateral cerebral arteries, which
pass one on each side to the cerebral ganglia
and discharge to other cephalic blood
spaces.

The venous spaces in the head all connect
with a main cephalic hemocoel lying round the
gut and cerebropleural and cerebropedal
connectives. At the level of the pleuropedal
ganglia a large pedal venous sinus passes
dorsally from the foot in the central space of
that group of four ganglia and joins the ce-
phalic hemocoel to form the cephalopedal si-
nus or vein, in which lie the esophagus, the
anterior aorta and the left half of the visceral
loop. Posteriorly this sinus enters the base of
the visceral mass just left of the roof of the
mantle cavity and receives venous sinuses
from the visceral mass. The combined vessel,
the afferent renal vein, though continuing
through the kidney as a conspicuous vein,
breaks up into a large number of branches
which form a plexus on the floor of the kidney.

Posteriorly the main vessel and the plexus
connect with a prominent efferent renal vein
running along the kidney wall on the left and
more dorsally. All blood returning from the
head-foot and visceral mass thus passes
through the kidney and collects in the efferent
renal. This vessel runs within the kidney al-
most to the most posterior level of the peri-
cardial cavity where it turns abruptly into the
ctenidial axis. Here it runs in a dorsal position
along the whole length of the gill, giving rise to
the vessels of the leaflets. These drain ven-
trally into the ctenidial efferent returning blood
to the heart.

Anteriorly extensions of the efferent renal
vein pass out of the kidney to form a plexus
round the rectum. This seems to be much bet-
ter developed in males than in females.

The pallial vein runs as a prominent vessel
bulging into the mantle cavity from the more
dorsal part of the mantle skirt, parallel to its
edge, along its whole length. Anteriorly it re-
lates to a small cluster of small lamellae that
may represent a vestige of the right ctenid-
ium. Near the point where it enters the auricle
it receives blood from a pallial vein running
parallel to it in the mantle edge which is fed
from the circumpallial artery.

The blood spaces throughout the body are
unusual in that all, down to the smallest, have
an endothelial lining of squamous cells.

Excretory system

Neomphalus has only one kidney, the left. It
is, however, more than just an excretory or-
gan and forms a capacious body cavity, deep
and wide. Indeed, it is more prominent as
body cavity than as kidney since little of its
surface seems to be involved in excretory ac-
tivity, and only where the lining cells overlie
the blood vessels in its walls (Fig. 7).

The kidney lies in the roof of the mantle
cavity and extends widely under the visceral
mass on the right, separating it from underly-
ing shell muscle. Its anterior boundary is
formed by shell muscle and its posterior
boundary coincides approximately with the
anterior wall of the pericardial cavity except
for a lobe projecting dorsal to it and a long,
narrow, horn-shaped canal which runs along
its left side and does not terminate until level
with the extreme posterior end of the auricle.
The kidney opens to the mantle cavity by a
pore with ciliated lips placed towards its left
margin. We have found no pericardial con-
nexion.

348 FRETTER, GRAHAM AND MCLEAN

Near the point where the anterior and pos-
terior aortae are formed by division of the bul-
bus, the right wall of the kidney gives rise to a
series of tubules which extend ventral to part
of the digestive gland and around the most
posterior part of the cephalopedal sinus. The
tubules open from the main chamber of the
kidney by small apertures but then immedi-
ately dilate and become pressed against
small arteries arising from the posterior aorta.
The whole produces a spongy mass of
spaces traversed by small blood vessels. This
part of the organ drains to a vessel which runs
on to the pericardial wall but which we have
not been able to trace further. This area of the
kidney corresponds to the nephridial gland oi
other prosobranchs.

The kidney is intimately related to a number
of other organs. The afferent renal vein,
formed from the fusion of cephalopedal and
visceral venous sinuses, becomes associated
with its ventral wall anteriorly and sends nu-
merous branches over it. On the right this
plexus drains to the efferent renal vein. This
connects anteriorly with vessels lying around
the rectum but runs mainly along the posterior
horn of the kidney to become the afferent
ctenidial vessel. The two visceral ganglia also
lie in the kidney wall, the right in proximity to
the efferent renal vessel, the left alongside the
afferent renal.

Histologically most of the kidney is covered
by a low cuboidal epithelium which may con-
tain yellow granules but has no other distinct
features. In some places—in the right exten-
sion under the visceral mass and in the ne-
phridial gland—the epithelium is squamous.
Wherever the cells overlie blood vessels,
however, their appearance is different: they
become columnar, have rounded apices very
often clearly in the process of being budded
off. There are few ciliated cells except in the
immediate vicinity of the external opening.

Nervous system

The nervous system (Fig. 8) is in most re-
spects a typical archaeogastropod one,
though it also has some advanced features. It
shows a primitive spread of nerve cells along
nerve tracts rather than wholly concentrated
into ganglia. Nerves, connectives and ganglia
are all closely associated with the vascular
system and almost without exception run in
venous spaces.

The cerebral ganglia (Fig. 9) are ovoid
bodies placed laterally and dorsally near the

FIG. 8. Plan of nervous system; dorsal view. The
black circle over the pedal ganglion marks the posi-
tion of a statocyst. ap, anterior pallial nerve from
branchial (osphradial) ganglion; bg, buccal gang-
lion; с, cardiac nerve; cc, cerebral commissure; сд,
cerebral ganglion; cpd, cerebropedal connective;
cpl, cerebropleural connective; ct, ctenidial nerve;
dn, nerve to dorsal cephalic body wall; g, nerve to
genital opening and anus; k, nerve to renal open-
ing; lo, nerve to left half of osphradium; lv, left vis-
ceral ganglion; on, oral lappet nerves; pa, anterior
branch of pallial nerve from subesophageal gang-
lion; pc, pedal cord; pp, posterior branch of pallial
nerve; ro, right osphradial nerve; rp, right pallial
nerve; rv, right visceral ganglion; s, nerve to shell
muscle; sb, subesophageal ganglion; sp, supra-
esophageal ganglion; tn, nerves to tentacle; va, an-
terior nerve to floor of mantle cavity; vp, posterior
nerve to same area; 1, 2, 4, 5, pedal nerves.

anterior end of the cephalic hemocoel and
linked by a stout commissure which passes
anterior (dorsal) to the buccal cavity at a level
ventral to the salivary pouches and dorsal to

ANATOMY OF NEOMPHALUS 349

А’ Mo

FIG. 9. Right cerebral ganglion, buccal ganglion and related nerves; ventral view. A, anterior; bc, buccal
commissure; ben, cerebrobuccal connective; bg, buccal ganglion; cc, cerebral commissure; ср, cerebro-
pleural and cerebropedal connectives; dn, nerve to dorsal surface of head; dt, dorsal tentacular nerve; L. left;
|, labial lobe of cerebral ganglion; In, labial nerve; lo, lateral nerve of oral lappet; m, mouth; mo, medial nerve
of oral lappet; P, posterior; R, right; tn, tentacular nerve.

the inner ends of the jaws. On its ventral face
each ganglion bears a labial lobe from which
the buccal connective arises, and posteriorly
it gives rise to a more dorsal cerebropleural
connective and a more ventral cerebropedal
one.

The following nerves originate from each
ganglion in addition to the connectives and
commissure.

From the main body of the ganglion:

1. Median nerve of the oral lappet, running
to its anterior face.

2. A very stout tentacular nerve with a
small dorsal branch.

3. A dorsal nerve from the base of the cer-
ebropleural connective to the skin of the
head.

From the labial lobe:

1. Lateral nerve of the oral lappet, running
to its posterior face.

2. (As a branch from the base of the cere-
brobuccal connective) a labial nerve
which divides into anterior and posterior
branches to the lips. Neither branch was
seen to join with its contralateral partner
to form a labial commissure.

The cerebropleural and cerebropedal con-
nectives run posteriorly, one dorsal to the
other, on the inner faces of the lateral walls of
the neck, lying in subsections of the cephalic
hemocoel. The pleuropedal ganglia are
placed just posterior to the point where neck
and foot join, alongside the beginning of the
posterior esophagus. A constriction separates
the more dorsal pleural from the more ventral
pedal part.

The right pleural ganglion tapers back-
wards and to the left and soon connects with a
prominent supra-esophageal ganglion. The
left pleural narrows backwards and to the right
and expands into a small subesophageal
ganglion. No nerves seem to issue from the
pleural ganglia (Fig. 10). The subesophageal,

350

yh)
S

FRETTER, GRAHAM AND MCLEAN

FIG. 10. Arrangement of nerves supplying gill, osphradium and mantle skirt; dorsal view. A, anterior; bg,
branchial ganglion; ct, ctenidial nerve in gill axis; L, left; lo, left part of osphradium; Ip, left pleural ganglion; lv,
left half of visceral loop; mc, posterior limit of opening of mantle cavity; P, posterior, pn, pallial nerve; R, right;
ro, right part of osphradium; rp, right pleural ganglion; rv, right half of visceral loop; sb, subesophageal

ganglion; sp, supra-esophageal ganglion.

however, gives off a large nerve to the right,
innervating part of the food groove and part of
the shell muscle. An extremely large nerve
Originates from the left side of the ganglion
and passes into the mantle skirt immediately
anterior to the branchial extension of the su-
pra-esophageal ganglion and very close but
ventral to nerves coming from that ganglion. It
divides into branches which run backwards
and forwards near the pallial edge.

The supra-esophageal ganglion is conflu-
ent with a prominent branchial or osphradial
ganglionic mass in the mantle skirt, from the
dorsal surface of which arises a thick ctenidial
nerve, containing many nerve cells. This runs
to the point of attachment of the ctenidial axis;
here it may be traced to the anterior tip of the
gill. lt becomes associated with an elaborate
plexus of small nerves lying on its right and
left sides; only this plexus extends along the
posterior portion of the gill axis. From the
base of the ctenidial nerve an osphradial
nerve runs to an osphradial area lying right of
the gill axis; another nerve, with a separate
origin from the branchial ganglion, goes to a
corresponding sensory area left of the axis
and also sends a small branch to the posterior
part of the mantle edge. A very large pallial
nerve passes forward from the branchial
ganglion to the pallial margin.

The left half of the visceral loop (Fig. 7) runs

posteriorly in the cephalopedal sinus to the
floor of the kidney alongside the anterior loop
of the intestine and the posterior esophagus,
expanding, shortly before it enters the kidney,
into an elongated visceral ganglion. The
right half of the loop runs amongst muscle
fibers on the left margin of the shell muscle
close to the anus and genital pore. It lies
nearly directly dorsal to the left half, especially
posteriorly where it enters the ventral wall of
the kidney and expands into an elongate right
visceral ganglion linked by a short commis-
sure to that on the left.

Some nerves originate from the visceral
connectives. On the left a small plexus of
nerves lies in the pallial floor with connexions
anteriorly and posteriorly to the connective;
another nerve, arising near the supra-esoph-
ageal ganglion, innervates the walls of the
cephalopedal sinus. Just anterior to the left
visceral ganglion a further nerve runs poste-
riorly into the pallial floor. On the right two
nerves leave the visceral connective near the
subesophageal ganglion and go to the food
groove, whilst another, leaving the connective
close to the point where it enters the kidney,
goes to the region of the anus and genital
pore. A large nerve to the shell muscle leaves
the anterior part of the right visceral ganglion
and a small one from its posterior end goes to
the lips of the kidney opening. A cardiac nerve

ANATOMY ОЕ NEOMPHALUS 351

originates from the left ganglion and runs in
the wall between kidney and pericardial cav-
ity.
The pedal ganglia form cords which run the
length of the foot, gradually diverging and be-
coming more slender. A prominent commis-
sure links them anteriorly and there are at
least three further connexions more poste-
riorly, giving a generally scalariform pattern.
Numerous nerves pass forward and laterally
from the cords innervating the posterior part
of the neck and the muscles and sense or-
gans of the foot.

A statocyst containing a single statolith sits
on the dorsal surface of each pedal ganglion.
No trace of any eye or optic nerve can be
found.

Reproductive system

In the male (Fig. 12) the testis lies on the
dorsal side of the visceral mass, covering the
right and posterior half. It is made of a series
of blind tubules which converge towards the
left anterior end of the organ on a short vas
deferens. Spermatogenesis was in active
progress in the animals examined and large
numbers of ripe sperm filled the tubules and
the duct. Only one type of sperm appeared to
be present.

The vas deferens discharges to the lumen
of an extremely large prostate gland which
occupies the left dorsal part of the visceral
mass; behind the vas deferens a narrow ex-
tension of the pericardial cavity lies between
prostate and testis. The gland has an anterior
and a larger posterior lobe, both formed of
tubules discharging to the main ducts. The
rather large central space of the gland leads
to the male pore placed between the rectum
dorsally and the right half of the visceral loop
ventrally, just anterior to the anterior end of
the kidney and more or less level with the
anterior shoulder of the shell muscle. The lips
of the pore spiral outwards and form the mar-
gins of a groove which runs for a short dis-
tance parallel and ventral to the rectum, grad-
ually flattening (Fig. 11A).

Ventral to the bulbus of the heart the wall of
the mantle cavity in males shows a small blind
diverticulum. This corresponds in situation
with the receptaculum seminis of the female
of which it seems be a rudimentary homo-
logue. This would seem to indicate some
hormonal control of its development.

In the female (Fig. 13) nearly the whole of
the dorsal surface of the visceral mass is oc-

FIG. 11. A, dissection of male, showing area
around male opening and anus; B, similar dissec-
tion of female. a, anus; cf, ciliated field linking open-
ings of oviduct and receptaculum; fg, food groove,
running from right side of neck (left in figure) to
deep part of mantle cavity (right in figure); fo, fe-
male (oviducal) opening; |, lips of male pore extend-
ing to the right, ventral to the rectum; me, mantle
edge; mo, male opening; ng, nephridial gland within
kidney; pv, pallial vein with accompanying pallial
nerve ventral to it; r, rectum; rk, rectum within kid-
ney; ro, opening of receptaculum; rs, rectal sinus,
communicating posteriorly with renal vessels; s,
receptaculum seminis seen by transparency; sm,
right shoulder of shell muscle; v, right half of vis-
ceral loop; vg, right visceral ganglion in floor of
kidney.

cupied by the ovary. Like the testis it is
formed of branching tubules and is bordered
on its left by a pericardial extension. The tub-
ules converge on a point on the left side of the
ovary, nearly at its extreme anterior end. At
this point the ovary opens, apparently without
the intervention of any ovarian duct, into the
first section of the female duct, the opening
lying at the centre of a ring-shaped fold; some
muscles run from its lips to the dorsal surface
of the mantle and may regulate passage of
eggs. A short and very narrow gonopericar-
dial duct runs from the point where ovary and
oviduct are linked to the innermost end of the
pericardial extension.

352 FRETTER, GRAHAM AND MCLEAN

FIG. 12. A, diagram of male reproductive system;
dorsal view; B, transverse section. D, dorsal; dg,
digestive gland; L, left; mo, male opening; pc, peri-
cardial cavity and its forward extension into the vis-
ceral mass; note the glandular epithelium against
the digestive gland; pr, prostate gland; R, right; r,
rectum by anus; sm, shell muscle; t, testis; V, ven-
tral.

The oviduct starts as a nearly globular
chamber with numerous folds on its walls, two
folds apparently separating it from the second
section of the duct. This runs backwards as a
smooth-walled tube along the left side of the
ovary but separated from it by the pericardial
extension until it is near the main pericardial
Cavity. Here it turns abruptly through 180° and
proceeds forwards, in contact with, and to the
left of the proximal section. This distal part of
the oviduct, like the initial part, has many folds
on its walls. There is also present a richly-
ciliated groove on its topographically right-
dorsal wall; this may be traced on to the left
wall of the proximal section where it opens out
to form a flat, ciliated tract running to its inner
end. Anteriorly, just in front of the connexion
between ovary and duct, the oviduct opens to
the mantle cavity, its lips out-turned to form a

FIG. 13. A, diagram of female reproductive system;
dorsal view; B, transverse section. c, ciliary tract in
roof of mantle cavity and in female duct; D, dorsal;
dl, distal limb of oviduct; dg, digestive gland; fc,
fertilization chamber; fo, female opening; L, left; о,
ovary; pc, pericardial cavity and its forward exten-
sion into the visceral mass, glandular epithelium
against the digestive gland; pl, proximal limb of ovi-
duct; R, right; r, rectum by anus; rs, receptaculum
seminis; sm, shell muscle; V, ventral.

lobed, bell-shaped structure (Fig. 11B) placed
in a position corresponding to that of the male
pore.

At a point anterior to and to the right of the
pore, between its lips and the shell muscle,
the ciliated groove opens to the front end of a
short ridged and grooved area which runs
back on the wall of the mantle cavity, ventral
to the edge of the kidney (Fig. 11B). At the
posterior end of this area lies a small opening
leading to a receptaculum seminis. Its duct is
ciliated and muscular, narrow near the open-
ing but widening as it runs transversely to the
right. The receptaculum lies under the ante-
rior end of the pericardial cavity and contains
spermatozoa, all lying with their heads
against the epithelium lining it (though not ap-
parently embedded in it) and their tails in a
central mass. In the mantle cavity of one spe-

ANATOMY OF NEOMPHALUS 353

cimen sectioned, near the receptacular open-
ing, small clumps of sperm were also found
but none were seen in any part of the oviduct.
These sperm were not related to any nurse
cell, nor were they organized into spermato-
phores or spermatozeugmata, though they
may well have had some prostatic secretion
around them.

The prostate gland contains two types of
cell, ciliated and glandular, which lie more or
less alternately to compose the epithelium.
The ciliated cells are wineglass-shaped with
long stalks attaching their expanded distal
parts, in which the nuclei lie, to the basement
membrane. The gland cells have broad bases
containing nuclei and some vacuoles, each
with a spherule of secretion; the base is con-
nected to a narrower apical part packed with
secretory granules. These stain a brilliant
orange with eosin and are shed to the lumen
of the tubules where they swell, stain red, and
ultimately dissolve. Ripe sperm, which have
long, narrow heads, fill the vas deferens and
parts of the main lumen of the prostate, em-
bedded in material of prostatic origin. In the
lumen of the prostate many sperm orientate
so that their heads lie towards the epithelium
and some, indeed, appear to become em-
bedded in the ciliated cells. The lips of the
male pore and its grooved extension along-
side the rectum are heavily ciliated.

The ovary of the animals examined seemed
active in every case and contained many ap-
parently ripe eggs. Some eggs were also
present in the proximal limb of the oviduct, but
this was interpreted as a post-mortem effect
rather than a normal process of egg shedding.
In this situation the eggs had a diameter of
100-150 um, were moderately rich in yolk but
had no external coats. The wall of the oviduct
consists throughout of alternating ciliated and
gland cells, except in the ciliated groove
where gland cells are absent. The deiails of
the cells, and of the secretion they elaborate,
however, differ from the one limb to the other.
In the proximal the ciliated cells are moderate-
ly broad at their free ends and the gland cells
rather narrow. The cytoplasm of the latter
contains many vacuoles and although much
of the secretion seems to have been lost on
fixation it is clear that it stained with hematox-
ylin. In the distal section of the duct the cili-
ated cells are extremely slender and the gland
cells very swollen. Their cytoplasm contains
usually only one large vacuole the contents of
which (though again mainly dissolved) stain
with eosin. Eggs, therefore, presumably re-

ceive two coatings as they pass along the
oviduct. Since the ciliated groove originates in
a tract related to the receptaculum it may be
supposed that sperm received from the male
and stored there are passed to the ciliated
groove along which they travel up the oviduct,
are liberated at the upper end of the proximal
limb where the tract to which the groove leads
comes to an end. This would represent the
site of fertilization, after which event the eggs
would be carried down the tract, receiving
their two coats as they go.

DISCUSSION

In its anatomy Neomphalus fretterae is
unique amongst living gastropods, presenting
a combination of archaic and advanced fea-
tures which effectively prevents its associa-
tion with any living group. It does not fit easily,
moreover, into the customary division of pro-
sobranchs into archaeogastropods and
mesogastropods (or caenogastropods, to use
Cox’s (1960) wider term) since, according to
the system used as criterion, it falls clearly
into the one group or equally definitely into the
other. Since this is obvious also in Trochacea
and the mesogastropods are not in them-
selves a markedly coherent group it suggests
strongly that the term mesogastropod refers
to a particular level of organization rather than
a single taxonomic division. In addition
Neomphalus has many features which relate
to its unusual mode of life and may well be
peculiar to itself.

Archaeogastropod characters. These are
exhibited most clearly in the ctenidium, which
is aspidobranch, and in the radula, which is
rhipidoglossate, even if in their detailed or-
ganization neither is exactly typical. Another
external feature linking Neomphalus to the
archaeogastropods is the presence of epipo-
dial tentacles, though their restriction to the
posterior part of the foot is unusual.

In internal anatomy, features of the alimen-
tary and nervous systems most clearly em-
phasize the archaeogastropod condition.
Small glandular pouches in the roof of the
buccal cavity are reminiscent of the salivary
glands of Diodora and are not very different
from the small tufts of all archaeogastropods
other than Patellacea. The buccal cavity also
contains a radular diverticulum from which the
radular sac opens. This feature occurs in
most archaeogastropods but is absent from

354 FRETTER, GRAHAM AND MCLEAN

mesogastropods. As in archaeogastropods
generally, there are lateral glandular pouches
along the whole length of the mid-esophagus
which anteriorly overlap the posterior part of
the buccal mass, whereas in mesogastropods
they lie posterior to it (Amaudrut, 1898). The
reduction in the degree of folding of their walls
may be partly compensated for by their in-
creased length. This part of the gut, too, which
ordinarily shows the effects of torsion by the
rotation of the folds on its walls, has come to
lie anterior to the region affected by torsion
and is symmetrical; this may well also be
linked with the elongation of the neck. The
presence of an anterior intestinal loop is an-
other archaeogastropod character.

The nervous system is hypoathroid to dys-
tenoid and shows many primitive characteris-
tics (Fretter & Graham, 1962). The cerebral
ganglia lie well forward in the head and far
apart, linked by a long commissure. They
connect with the pleural and pedal ganglia by
connectives which, even allowing for the ex-
tension of the neck, are long. The pleuropedal
ganglia form a connected but clearly bilobed
mass on each side and the pedal ganglia take
the form of elongated cords connected across
the mid-line by several commissures. The
visceral loop is normal in arrangement except
for the tightness of the streptoneury around
the esophagus and some points in the distri-
bution of the nerves dealt with later. Many
cells lie in nerves.

Mesogastropod characters. In contrast to
these features there are some points in the
anatomy of Neomphalus which agree with
mesogastropods rather than with archaeo-
gastropods, and in some systems the ar-
rangement is wholly mesogastropodan.
Though the arrangement of muscles in the
buccal mass is in some respects—more раг-
ticularly in relation to the transverse fold—like
that of archaeogastropods, it is in total rather
more mesogastropod than archaeogastropod
in character. This is particularly obvious in the
reduced number of muscles which are pres-
ent by comparison with, for example, a trochid
(Nisbet, 1973) or patellid. The gut is also
clearly mesogastropod in that the rectum
does not enter the pericardial cavity, let alone
penetrate the ventricle.

In the nervous system the cerebral ganglia
have each a ventrally placed labial lobe,
representing the originally separate labial
ganglion. In archaeogastropods this fusion
has not occurred, and a labial commissure,

absent in Neomphalus, is usually present.
The statocysts each contain only a single
statolith as in mesogastropods, whereas
there are normally several in archaeogastro-
pods.

Although the ctenidium is aspidobranch it is
single, the right one having apparently all but
disappeared, and with it the right auricle of the
heart.

The mesogastropod resemblances of
Neomphalus are clear in the renal and repro-
ductive systems. There is only one kidney, the
left; any persistent part of the right kidney has
become incorporated in the reproductive tract
and has no excretory significance. The left
kidney is very similar in organization to that of
a monotocardian and is neither a papillary sac
as in pleurotomariaceans and trochaceans
nor reduced as in patellaceans and fissurel-
laceans. Indeed the kidney expands (as in
some rissoacean mesogastropods) to form a
large body cavity into which gut, blood ves-
sels and visceral ganglia project. It forms a
space separating shell muscle from viscera
and penetrates, along with outgrowths from
the pericardial cavity, amongst the viscera, so
that there is an extensive coelomic space
throughout the visceral mass. Perhaps as a
consequence of its increase in area the kid-
ney wall is simple, almost completely lacking
the folds common in other prosobranchs, and
evidence of excretory activity is largely limited
to sites overlying the renal vessels.

The nephridial gland, though conforming in
general to the structure it exhibits in proso-
branchs, is unusual in that it is much more
spongy, the tubular projections of the kidney
being inflated and the related vessels reduced
in size, though numerous.

The structure of the auricle suggests that a
primary urine might be filtered through its
walls, and the gland cells which line the peri-
cardial cavity where it abuts against the blood
spaces of the digestive gland show signs of
nipping off parts of the cell tip. It is surprising,
in the light of these facts, that there seems to
be no renopericardial opening through which
filtrate and secretion might pass to the kidney.
Expectation of finding one at the posterior end
of the horn-like prolongation of the kidney
towards the base of the auricle was high,
since that is the position in which it would
normally be found, but there is certainly no
renopericardial papilla, though it is still possi-
ble that some relatively inconspicuous con-
nexion exists which has eluded our search.
The explanation of the presence of this poste-

ANATOMY OF NEOMPHALUS 355

rior extension—if it does not lead to a reno-
pericardial opening—may be to lead the renal
efferent to the base of the gill.

The relationship of kidney and vascular
system is typically monotocardian with all the
blood from head-foot and visceral mass being
passed through the kidney; from this it col-
lects into an efferent vessel and passes into
the ctenidial axis or a rectal sinus, in both of
which places it may be oxygenated. Neom-
phalus differs from mesogastropods in that
the breakdown of the afferent renal vessel to
form a plexus is less complete and a rather
large vessel runs to link with the efferent.

Characters peculiar to Neomphalus. The head
has no pretentacular elongation with the re-
sult that mouth and tentacles are terminal.
There is, however, a very marked post-tenta-
cular elongation which brings these structures
far in front of the anterior edge of the foot. This
neck region bears lateral expansions reminis-
cent of the neck lobes of a calyptraeacean,
and, to a lesser extent, of a trochacean. The
homologies are doubtful. Neck lobes in tro-
chaceans are considered to be forward ex-
tensions of the epipodium and in calyptraea-
ceans of the propodial region of the foot. In
Neomphalus some posterior parts of the
lobes are innervated from the pedal ganglia
and others from the subesophageal, but the
anterior region is supplied by nerves from the
cerebropedal connectives and, to a minor ex-
tent, from the cerebral ganglia.

Neck formation has affected internal or-
gans, elongating the cerebropleural and
cerebropedal connectives and cephalic ar-
tery. It has also affected the course of the
protractor muscles of the radular membrane.
In most prosobranchs these run posteriorly to
join the columellar muscle (as in trocha-
ceans), or the shell muscle (as in patella-
ceans); in proboscidiferous forms they short-
en and originate in the lateral walls of the
head. In Neomphalus elongation of the neck
seems to have acted like a post-tentacular
proboscis and brought about the same result.
The mid-esophagus normally lies in the re-
gion of torsion: in Neomphalus it lies anterior
to it. This anterior migration may well have
been a consequence of elongation of the
neck.

The stomach is relatively simple in organi-
zation though most features of prosobranch
gastric anatomy apart from sorting areas are
present in standard topographical relation-
ships though reduced form. In its histology,

however, an unusual feature is the arrange-
ment of cells involved in the formation of the
gastric shield. The small tubular outgrowth at
the apex of the stomach has characteristics
agreeing with those of a spiral caecum and
also has a sufficiently correct spatial relation-
ship with the gastric shield to suggest ho-
mology with that structure. Reduction of this
part of the stomach also occurs in Fissurel-
lacea and Patellacea and may therefore be
connected with the adoption of a limpet shape
and simplification of the visceral coils.

The digestive gland is relatively small and is
peculiar in being confined to the topographi-
cal underside of the visceral mass. Its struc-
ture appears unusual in the apparent pres-
ence of tubular glands in the tubules.

The ctenidium is unique—a bipectinate gill
of extraordinary length, unattached on its af-
ferent side, though the axis is stoutly and
broadly fastened to the mantle skirt along
most of its length and supported by a hyper-
trophy of skeletal tissue. The lamellae have
elongated into filaments, well ciliated, and the
whole adapted for creating and sieving a wa-
ter stream.

The most outstanding features of Neom-
phalus are its limpet-like form and the en-
largement of the mantle cavity and gill to allow
ciliary food-collecting, changes which have af-
fected the visceral half of the body to a greater
extent than the head-foot.

Three major alterations in organization
have accompanied the adoption of the limpet
shape: (1) the pallial organs of the animal's
right side have disappeared except for a ves-
tigial ctenidium and an associated vessel
which remains well developed because it has
assumed the drainage of the expanded man-
tle skirt; (2) the visceral mass has undergone
270° of torsion in relation to the head-foot;
(3) the mantle cavity and visceral mass have
undergone a leftward rotation about an an-
teroposterior axis so that structures originally
right have moved dorsally and those originally
left, ventrally. Much of the palliovisceral ana-
tomy—and some of the cephalopedat—can
be explained in terms of these movements.

The loss of topographically right pallial or-
gans is clear so far as osphradium and kidney
are concerned. The loss of the right ctenidium
is equally as obvious at first sight as it is in the
monobranchiate patellaceans, yet a vestige
seems to persist. Near the mouth of the man-
tle cavity, anteriorly and to the left of the mid-
line, a group of 5-10 ciliated lamellae lies over
the course of the pallial vein. This vessel runs

356 FRETTER, GRAHAM AND MCLEAN

posteriorly to the innermost part of the mantle
cavity where it turns forward to join the effer-
ent branchial and so the auricle. In typical
archaeogastropods only three vessels run to
the auricles: two efferent branchials, one to
each auricle, with the nephridial gland efferent
joining that on the left. In Neomphalus there is
no right auricle, but two vessels from opposed
parts of the mantle skirt enter the left one (the
course of the nephridial gland efferent re-
mains unclear but neither vessel can be that).
It is, therefore, in view of these relationships,
appropriate to assume that the pallial vein is
homologous with the right ctenidial efferent,
secondarily associated with the left one in
view of other changes (see below). The idea
of an efferent ctenidial vessel persisting even
in the absence of a functional gill is support-
ed by the presence of the right pallial vein in
trochids.

There are not many situations in the body of
a prosobranch gastropod where one regularly
finds a prominent blood vessel and an equally
prominent nerve lying alongside one another,
especially within the confines of the mantle
skirt. The ctenidial axis is one such place and
it was initially the close association between
the pallial nerve and the pallial vein which first
led us to ask whether this vessel might be
related to a lost gill.

Two facts bear against this interpretation. In
the left ctenidial axis, anteriorly, the ctenidial
nerve lies under the efferent vessel; it origi-
nates in the supra-esophageal ganglion.
Alongside the pallial vein, the putative right
ctenidial efferent, there also runs a prominent
nerve, as one would expect if this is the cor-
rect homology. This nerve, one would sup-
pose, should connect with the subesophageal
ganglion. It does not, however, and proves to
be a branch from the supra-esophageal. The
second fact is the situation of the vessel in the
mantle skirt. In Fig. 16A, the morphologically
mid-ventral line of the mantle cavity is marked
by the esophagus, its morphologically mid-
dorsal line by the rectum. The right half of the
mantle skirt is compressed to the small part
between rectum and esophagus in which the
genital duct lies. If the pallial vein were a right
ctenidial efferent, and if it retained its original
situation, it should be found here too; yet it lies
morphologically left of the rectum.

There are thus some points—association of
nerve and vessel, lamellae, relationship to
heart—which speak for the homology, and
others—innervation, situation on mantle
skirt—which argue against it. There seems no

way to resolve the matter on present knowl-
edge.

The existence of 270° of torsion instead of
the usual 180° has the effect of making the
long axis of the visceral mass lie at right an-
gles to that of the head-foot instead of parallel
to it, and of bringing the original left edge of
the mantle cavity to the posterior end of the
body. This is immediately seen on looking at
an animal removed from its shell in dorsal
view. Then it is obvious that the attachment of
the shell muscle is indeed horseshoe-shaped
as in other limpets, but its concavity faces left,
not anteriorly. When that displacement is al-
lowed for, the disposition of the organs of the
visceral mass becomes nearly identical with
that of other prosobranchs, the pericardial re-
gion alongside one end of the horseshoe, the
anus and genital opening alongside the other.

Torsion makes itself evident not just in the
orientation of the visceral mass but in the
twisting of gut and visceral loop. With т-
creased torsion this effect should be more
marked, and this is indeed so, the twisting of
the visceral loop round the esophagus being
extremely tight and accomplished within a
very short distance. This may, perhaps, be an
additional factor in bringing about the forward
migration of the mid-esophagus, which leaves
only the much narrower posterior part to be
embraced by the connectives.

It is not, however, possible to explain all the
anatomical peculiarities of the visceral and
pallial parts of Neomphalus on the basis of
the two changes just mentioned. They leave
unexplained the disposition of the esophagus
and visceral nerve loop, the heart, the stom-
ach, the digestive gland, gonad and genital
duct, and the position of the ctenidium and
(right) pallial efferent. To understand how
these have come to be as they are, a third
movement has to be introduced—a roll round
an anteroposterior axis of visceral mass and
mantle to the left, which in effect shifts the
mantle cavity from a dorsal to a left lateral
position. That this has occurred is clearly
shown by examination of the stomach and the
heart.

The stomach of a typical prosobranch is
fundamentally U-shaped, the concavity facing
forwards, the esophagus opening anteriorly to
the left limb whilst the intestine runs forward
from the right (Fig. 14). The spiral caecum, if
present, opens from the apical region. In
Neomphalus the stomach is still U-shaped but
the concavity faces left because of the in-
creased torsion. The positions of esophagus

ANATOMY OF NEOMPHALUS 357

FIG. 14. Diagrams to show the topographical rela-
tionships between the stomach of a primitive pro-
sobranch such as a trochacean and that of Neom-
phalus. 1, dorsal view of the stomach of an animal
such as Monodonta; 2, the same after rotation
through 180° on an anteroposterior axis; 3, after a
further 90° rotation anticlockwise on a vertical axis,
the consequence of increased torsion; 4, diagram
of the stomach of Neomphalus, comparable to dia-
gram 3 with the intestine running forward to the
anus. Gastric shield hatched; area of ducts of di-
gestive gland stippled. A, anterior; c, spiral caecum;
e, esophagus; i, intestine; L, left; P, posterior; R,
right.

and of rectum and anus, however, remain
unchanged—anterior to the stomach, and left
and right respectively. The esophagus opens
into the anterior limb of the stomach and the
intestine arises from the posterior. If the posi-
tion of the stomach were simply due to a ro-
tary motion these positions would be re-
versed. The actual anatomy can be explained
only on the assumption that the stomach has
also turned over so that the original dorsal
surface is now underneath. This movement
also explains how the dorsal surface of the
visceral mass is completely covered by gonad
whilst digestive gland is confined to its ventral
surface.

There are some unusual features in the or-
ganization of the heart region: the auricle lies
behind rather than anterior to tne ventricle,
the ctenidial efferent enters the auricle poste-
riorly and the bulbus lies at the anterior end of
the ventricle. Some of these features (position
of auricle and ctenidial efferent) can be attri-
buted to the shift due to increased torsion, but
not the details of the ventricle and aortae. In

the more primitive diotocardians with spirally-
coiled visceral humps, e.g., Pleurotomaria,
Scissurella, trochids, but not in the modified
fissurellaceans, the heart lies across the body
with the left auricle on the anterior side, the
right posteriorly and the aortae issuing from
the left side of the ventricle (Fig. 15). Apply
the two movements which have already been
described in relation to the stomach to such a
heart and an arrangement is reached which
differs from that in Neomphalus only in that a
right auricle is still present, receiving the right
ctenidial (or pallial) vessel. To achieve identity
with Neomphalus it has only to be supposed
that this vessel, and perhaps also its auricle,
migrate to join the left ctenidial efferent where
it enters the pericardial cavity.

This movement also brings the right pallial
vessel to a position approximately that oc-
cupied т Neomphalus. It would also cause
the attachment of the left gill to the mantle
skirt to lie on the floor of the mantle cavity as it
is found to do. It may, too, underlie the un-

FIG. 15. Diagrams to show the topographical rela-
tionships between the heart and associated struc-
tures of a primitive prosobranch and those of
Neomphalus. 1, dorsal view of heart and related
organs, based on Monodonta; 2, the same after
rotation through 180° on an anteroposterior axis; 3,
after a further 90° rotation anticlockwise on a ver-
tical axis, the consequence of increased torsion; 4,
diagram of Neomphalus, comparable to diagram 3,
save that the rectum (r) no longer enters the peri-
cardial cavity, the right auricle is lost and its associ-
ated vessel (p) now joins the efferent branchial (b).
A, anterior; a, anterior and posterior aortae arising
from bulbus; b, efferent branchial vessel running to
left auricle; L, left; P, posterior; p, pallial vessel; R,
right; r, rectum; v, ventricle.

358 FRETTER, GRAHAM AND MCLEAN

usual course of the large pallial nerve which
originates from the subesophageal ganglion.
This one would expect to run to the right,
whereas it runs to the left in close contact with
nerves from the supra-esophageal ganglion.
It may, however, still be directed at right pallial
organs now on the left because of these
topographical changes. One further anatom-
ical peculiarity of Neomphalus attributable to
this rotary movement shows that it has also
affected the posterior end of the head-foot
where that passes into the visceral mass. The
cephalopedal sinus, with its contained ante-
rior aorta, posterior esophagus and anterior
intestinal loop, appears unusually sited along
the left side of the shell muscle and the part of
the body linking head and visceral mass. An-
other odd feature of this part of the body is the
disposition of the visceral loop, the two halves
of which lie, not side by side as is usual, but
more or less in a dorsoventral plane, the right
half dorsal to the left. This abnormal arrange-
ment is easily understood on the supposition
that a leftward rotation of the mantle cavity
through about 90° has occurred. The original
mid-dorsal surface of the body (the floor of the
mantle cavity), marked by the aorta and
esophagus, now faces left instead of dorsally
and the visceral loop is brought into a vertical
instead of a horizontal plane (Fig. 16).

From these points it is clear the Neom-
phalus has followed an evolutionary course
quite different from those giving rise to the
fissurellacean and patellacean limpets, where
the mantle and visceral mass retain an an-
teroposterior alignment coincident with that of
the head-foot, or indeed, from that of any
other living mollusc. As a consequence the
pallial cavity—and to some extent the vis-
cera—come to lie on an axis parallel to but
alongside that of the head-foot, the right side
of the cavity in the same dorsoventral plane
as the left side of the foot. This gives a lower
shell than is encountered in other limpets, per-
haps an adaptation to the environment in
which the animals live, perhaps a reflection of
weaker powers of adhesion.

As might be expected from the common
adoption of a ciliary food-collecting mech-
anism there is a greater resemblance be-
tween Neomphalus and the hipponicacean
and calyptraeacean limpets, but these too re-
tain the basic relationship between head-foot
and visceral mass. Elongation of the mantle
cavity to permit a longer ctenidium has been
achieved by backward growth of its left side
only, unaccompanied by rotation or increased

FIG. 16. Diagrammatic transverse sections based
on camera lucida drawings to show the relative dis-
positions of mantle cavity, cephalopedal mass,
shell muscle, and certain organs. A, Neomphalus;
B, Diodora; C, Calyptraea. a, anterior aorta in
cephalopedal sinus; b, efferent branchial vessel in
gill axis, the osphradium alongside in A and В; с,
ctenidial leaflet; d, digestive gland; e, esophagus in
cephalopedal sinus; en, endostyle; f, foot; fg, food
groove; g, in A, the female opening; in B, the pro-
jection of the urinogenital opening on the plane of
the section; in C, the gonadial area of the visceral
mass; r, rectum; s, shell muscle; t, epipodial ridge;
v, visceral loop in cephalopedal sinus.

torsion. The ventricle has retained its central
position whilst the auricle has elongated
backwards to keep pace with the growth of
the gill. In Neomphalus this growth of the left
side has not occurred. Indeed in keeping part
of the mantle cavity over the head, it is the
anterior right part of the pallial margin which

ANATOMY OF NEOMPHALUS 359

has had to be extended. For this to happen,
retention of the right pallial vein may have
proved essential.

If the filaments of a ctenidium are to func-
tion well as a filter (Yonge, 1938) the axis
must be long (to allow filament number to in-
crease) and the filaments must elongate (to
allow current force and filtration area to grow).
In addition there must be some pathway to
carry filtered material to the mouth. in all pro-
sobranch ciliary feeders the collected food is
transported to the tips of the filaments and so
the pathway to the mouth lies on the side of
the body opposite to that from which the
ctenidial axis arises. These arrangements are
clear in the monotocardian ciliary feeders and
in Umbonium, the only archaeogastropod so
far described with this mode of feeding (Fret-
ter, 1975). Umbonium, however, is a trochid
and the bulk of its ctenidium is pectinibranch.
In all these animals a single rank of filaments
connects with a food groove. It seems that
these requirements could not be adequately
met in any aspidobranch retaining both right
and left ctenidia. It is presumably such me-
chanical difficulties that have led to the sup-
pression of the right ctenidium of Neom-
phalus. Its remaining gill functions well as a
filter only because of a modification of the po-
sition of its axis so that both sets of filaments
can lie across the mantle cavity and their tips
reach the food groove. The speculations of
Yonge (1947) and Fretter & Graham (1962)
that modification of a bipectinate gill for filter
feeding was highly improbable and that this
had to await the evolution of the monopec-
tinate condition have thus been proved un-
founded.

In typical archaeogastropods—not nerita-
ceans—the gonad discharges to the right kid-
ney, and any accessory secretion is produced
by the swollen lips of the opening of that or-
gan to the mantle cavity; from this comes the
jelly-like material in which the eggs of an ani-
mal like Calliostoma are deposited. The re-
productive system of Neomphalus, like that of
neritaceans, has reached the mesogastropod
level of complexity in that there is a glandular
region interposed between the gonad and the
genital opening, implying the occurrence of
some copulatory process and the laying of
some kind of spawn. There is, in conjunction
with the former, provision for the reception of
sperm by the female and for their transport to
an internal site of fertilization, necessitated by
the later provision of coatings which would
make union of egg and sperm difficult or im-

possible. It is to be noted that the glandular
section of the genital duct, in both sexes, is
closed, a condition more advanced than that
found in a number of mesogastropods.

Some discussion of the homologies of the
genital tract is necessary. The position of the
gonopericardial duct in the female shows that
there is no ovarian duct. And, though there is
no gonopericardial connexion in the male
(despite the presence of a similar pericardial
extension), it may be presumed that there is
no testicular duct either; however, absence of
a gonopericardial duct is usual in male caeno-
gastropods. Since the testicular duct of
mesogastropods is the site of sperm storage,
Neomphalus has, in its absence, come to use
the rather capacious lumen of the prostate for
this, and there are indications that some nutri-
tion of the sperm may occur there.

It is difficult to be certain of homologies in
the female and of how much, if any, of the
oviduct is pallial in origin. The proximal limb,
however, may be comparable with the albu-
men gland of mesogastropods, its expanded
upper part acting also as fertilization cham-
ber; the distal limb may correspond to the jelly
or capsule gland, with the ciliated groove
representing the ventral channel moved to its
present position by the roll of the mantle cav-
ity to the left which has already been теп-
tioned.

The homologies of the receptaculum
seminis are more obscure and the problem is
made more awkward in that the organ ap-
pears to act not only as a pouch for the recep-
tion of sperm (a bursa copulatrix) but also as a
storage place for them (а receptaculum
seminis). AS an anatomical structure, how-
ever, it is probably not homologous with the
structures of mesogastropods commonly
called receptaculum seminis since they lie in
most animals proximal to the oviducal glands.
A more likely homology is with the pouch
known as the bursa copulatrix. This is usually
distal to the glands and is the starting point of
the ciliated groove leading sperm to the site of
fertilization. The receptaculum of Neom-
phalus shows both these characters and to
complete the comparison it has only to be
supposed that it happens to have a situation
more remote from the female aperture than
usual. Though it is unlikely, because of their
relationship to the vascular system (Fretter,
1965), that the ducts of neritaceans are strictly
homologous with those of Neomphalus, sep-
arate openings of oviduct and receptaculum
are already known in that group. It may in-

360

deed be that this is the original site of a pouch
for reception of sperm and that its commoner
association with the oviduct is a secondary
position representing a tidying up in the man-
tle cavity or a consequence of the evolution of
the more efficient copulatory organ of the
mesogastropods.

A few deductions as to the activities of the
living limpet may be hazarded on the basis of
its anatomy. The foot is muscular enough to
suggest some locomotor as well as adhesive
activity. Although the radula is relatively short,
its structure and that of the buccal mass, along
with the contents of the gut, support the idea
that the limpet may supplement the food that it
collects on its gill by rasping the substratum.

In considering the mechanics of a copula-
tory process on the assumption that the left
tentacle of the male is a copulatory organ,
though not necessarily an erectile one, it has
to be remembered that it is not the oviducal
opening which the tentacle has to reach, but
that of the receptaculum. This lies on the left
side of the body in the wall of the kidney and
pericardial cavity about level with the anterior
end of the bulbus and ventral to it. It is there-
fore some distance behind the posterior limit
of the entrance to the mantle cavity. There are
several possible copulatory stances that ani-
mals might adopt—alongside one another,
heads together or at opposite ends; head on;
or, as is uSual in prosobranchs, with the male
mounted on the shell of the female, both fac-
ing in the same direction. Consideration of
each of these in relation to anatomy strongly
suggests that the last is by far the most likely,
and that the natural backward inclination of
the tentacle hooked over the thin, flat edge of
the shell would then bring it close to the open-
ing of the receptaculum. The vascular supply
to the tentacle is not great, indicating little
erectile capacity whereas it seems distinctly
muscular and it could presumably be pushed
further into the mantle cavity by some bending
of the neck. Since there is only slight indica-
tion of a seminal groove over its surface the
prostatic secretion must be sufficiently vis-
cous to prevent its general dispersal by the
currents in the mantle cavity.

There remains the problem of how sperm
reach the tentacle from the male pore since
there seems to be no direct link, and any such
would have to cross the food groove. The lips
of the pore, however, directly overlie the pos-
terior end of the groove along the left side of
the neck which leads to the tentacle, and it
seems possible that at copulation the one

FRETTER, GRAHAM AND MCLEAN

could become adpressed to the other, allow-
ing sperm to pass. We have, in addition, sus-
pected some extension of this groove on to
the dorsal surface of the neck on the left, ven-
tral to the food groove, which might facilitate
movement of seminal fluid.

In females the left neck groove is as well
marked as it is in males but is almost certainly
not involved in the outward passage of eggs.
It is not, however, apparently without function
since masses of material have been found
within it, mainly detrital. The most likely activ-
ity—which would occur in both sexes except
when copulation is occurring—is the removal
of particulate waste which has settled on the
floor of the mantle cavity before reaching the
ctenidium. This would correspond to the cur-
rent A described by Yonge (1938). The
groove is heavily ciliated and its epithelium is
rich in gland cells. Material collected here
would be embedded in secretion, led to the
left tentacle and dropped on to the substra-
tum.

It seems that fertilization of the eggs must
be internal, since a ciliated tract can be traced
from the mouth of the receptaculum to the
inner end of the proximal limb of the oviduct.
The fertilized eggs are then surrounded by
first, nutritive albumen, and then a protective
coat which seems more likely to be jelly-like
rather than of the nature of a capsule. But it is
not possible to say whether this is dispersed
outside the mantle cavity to free the eggs or
whether it is used to attach spawn to the sub-
stratum.

Finally, we attempt to assess the taxonomic
standing of Neomphalus on the basis of its
anatomy.

We have noticed only four features of
Neomphalus that are otherwise found only in
animals classified as Archaeogastropoda.
These are: the rhipidoglossate radula, the
radular diverticulum, the overlap of eso-
phageal pouches anteriorly with the buccal
mass, and the anterior loop of the intestine. It
possesses, it is true, other characters which
are commonly regarded as typical of archae-
ogastropods but these are actually also found
in some or many mesogastropods. The bi-
pectinate ctenidium is one of these—it is also
found in Valvatacea; the hypoathroid to dys-
tenoid nervous system is a second, but this
may also be seen in Cyclophoracea and Vi-
viparacea; epipodial tentacles represent a
third such character, but these are common in
mesogastropods in relation to the opercular
lobes, thus showing the same tendency as in

ANATOMY OF NEOMPHALUS 361

Neomphalus to disappear anteriorly whilst
persisting posteriorly. Anterior epipodial ves-
tiges may also perhaps be represented by the
neck lobes of cyclophoraceans and vivipa-
raceans. These three characters, therefore,
are shared by Neomphalus and some of the
lowest superfamilies of the mesogastropods.
There are, indeed, some other features in
which they agree: thus although in the cy-
clophoracean Pomacea canaliculata (An-
drews, 1965a, 1965b) there is no anterior
loop, the intestine runs so as to project into
the cavity of the kidney, as in Neomphalus,
rather than the digestive gland as is more
more usual; Pomacea also lacks a pretenta-
cular snout and so has a terminal mouth on
each side of which lies an oral lobe; in vivi-
parids, as in Neomphalus, it is a tentacle
which acts as copulatory organ, though the
right one rather than the left.

In all other respects the organization of
Neomphalus is unequivocally mesogastropod
and an enumeration of mesogastropod char-
acters would heavily outweigh the archaeo-
gastropod list. In these circumstances it
seems necessary to ask—is Neomphalus a
mesogastropod?

It must be borne in mind that the assump-
tion of mesogastropod characteristics is noth-
ing new in archaeogastropods—this is al-
ready evident in trochaceans. But members of
that group still retain a large number of fea-
tures in respect of which they agree with ar-
chaeogastropods rather than with mesogas-
tropods: two auricles, two kidneys, epipodial
sense organs, little or no development of
glandular genital ducts, none of which are
seen in Neomphalus. The same trend is obvi-
ous, and even more marked, in Neritacea,
whilst an examination of animals in the lowest
superfamilies of prosobranchs normally clas-
sified as mesogastropods shows a persist-
ence of features often regarded as archaeo-
gastropod. The requirements of the taxono-
mist make boundaries between groups more
rigid than they really are and there is no hard
and fast boundary between the archaeogas-
tropod and the mesogastropod groups. In
prosobranch evolution it is clear that numer-
ous and diverse attempts have been made by
different phyletic lines to pass from the level of
organization described by the term archaeo-
gastropod to that described by the term
mesogastropod. Most have ended in failure,
pushed into extinction by the radiation of the
successful monotocardians. Neritacea are an
exception and have succeeded in a radiation

predominantly in brackish and fresh water
and on land; Valvatacea have all but disap-
peared, while Architaenioglossa (Cyclo-
phoracea + Viviparacea) have been modestly
successful only by adopting some particular
and occasionally difficult habitats. Neom-
phalus seems to represent still another ar-
chaic group which has survived by adaptation
to a way of life allowing its persistence in a
very special habitat. On balance, however, it
seems to be further from the archaeogastro-
pod condition than are the groups referred to
above and accepted by most malacologists
as mesogastropods.

REFERENCES CITED

AMAUDRUT, A., 1898, La partie antérieure du tube
digestif et la torsion chez les mollusques gastér-
opodes. Annales des Sciences naturelles, Zo-
ologie, (7) 8: 1-291.

ANDREWS, Е. В., 1965a, The functional anatomy
of the gut of the prosobranch gastropod Poma-
cea canaliculata and of some other pilids. Pro-
ceedings of the Zoological Society of London,
145: 19-36.

ANDREWS, E. B., 1965b, The functional anat-
omy of the mantle cavity, kidney and blood sys-
tem of some pilid gastropods (Prosobranchia).
Journal of Zoology, 146: 70-94.

ANDREWS, E. B., 1979, Fine structure in relation
to function in the excretory system of two species
of Viviparus. Journal of Molluscan Studies, 45:
186-206.

COX, L. R., 1960, Thoughts on the classification of
the Gastropoda. Proceedings of the Malaco-
logical Society of London, 33: 239-261.

FRETTER, V., 1965, Functional studies of the
anatomy of some neritid prosobranchs. Journal
of Zoology, 147: 46-74.

FRETTER, V., 1975, Umbonium vestiarium, a filter-
feeding trochid. Journal of Zoology, 177: 541-
552.

FRETTER, V. & GRAHAM, A., 1962, British Proso-
branch Molluscs. London, Ray Society, xiv +
755 p.

MCLEAN, J. H., 1981, The Galapagos Rift Limpet
Neomphalus. Malacologia, 21: 291-336.

NISBET, R. H., 1973, The role of the buccal mass
in the trochid. Proceedings of the Malacological
Society of London, 40: 435—468.

YONGE, C.M., 1938, Evolution of ciliary feeding in
the Prosobranchia, with an account of feeding in
Capulus ungaricus. Journal of the Marine Bio-
logical Association of the United Kingdom, 22:
453—468.

YONGE, С. M., 1947, The pallial organs in the as-
pidobranch Gastropoda and their evolution
throughout the Mollusca. Philosophical Trans-
actions of the Royal Society of London, ser. B,
232: 443-517.

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MALACOLOGIA, 1981, 21(1-2): 363-369

EVOLUTION OF LARVAL DEVELOPMENT IN EASTERN ATLANTIC TEREBRIDAE
(GASTROPODA), NEOGENE TO RECENT

Philippe Bouchet

Museum National d'Histoire Naturelle
55, rue Buffon, 75005 Paris, France

ABSTRACT

Four lineages of eastern Atlantic Terebridae from the Miocene to Recent are discussed. The
type of larval development, as determined from observations of protoconchs, shows three kinds
of evolution through time: 1. loss of the planktonic stage followed by allopatric speciation;
2. size increase of the veliger larva; 3. planktonic development retained unchanged, followed

in one case by allopatric subspeciation.

It is suggested that there is no direct relation between dispersal capacity and a species’
temporal longevity. However, the limited evidence presented in the paper supports the idea that
allopatric speciation is connected with nonplanktonic larval development.

INTRODUCTION

Gastropod protoconchs yield information
on the type of larval development. This infor-
mation is used in alpha taxonomy by both
paleontologists and zoologists and the bio-
logical and evolutionary importance of the de-
velopmental stages has been the subject of
various papers (Thorson, 1946, 1961; Schel-
tema, 1966, 1971, 1972, 1977a; Robertson,
1976, among others).

It has been suggested (Scheltema, 1977b)
that prosobranch gastropods with long dura-
tion (teleplanic) planktonic larvae can main-
tain genetic exchange over long distances
and that these species are least liable to
change and speciate through time. Further-
more, it has been suggested that prosobranch
gastropods with more restricted capacity of
dispersal (medium to short duration plank-
tonic larvae) “will show geographic variation
and varying degrees of speciation” (Schel-
tema, 1977b: 317). Finally, species with direct
development are held to have a more re-
stricted range through space and time (Han-
sen, 1980).

There are only six documented cases of in-
traspecific variation in mode of reproduction
among prosobranchs (Robertson, 1976) and
in this paper the type of larval development
will be considered intraspecifically constant.

The distance factor has been investigated
in Recent species and it is known that through
planktonic larvae gene flow can be main-
tained between populations of a species living

on both sides of the Atlantic (Scheltema,
1971; Robertson, 1964).

The time factor has been much less inves-
tigated. The primary reason is that few line-
ages of fossil marine gastropods have been
adequately described. Most paleontological
studies are concerned with the whole gas-
tropod or mollusc fauna of a given locality,
with little or no concern with lineages. The
larval shells have been used, mainly in alpha
taxonomy, in only a small number of works. It
was not until Shuto (1974) and Scheltema
(1977b) that protoconchs became a subject of
theoretical interest in the study of proso-
branch evolution.

In this paper, | will discuss the lineages of
Eastern Atlantic Terebridae from Miocene to
Recent, with emphasis on the evolution of
types of larval development. In all cases, the
type of larval development has been deter-
mined through protoconch morphology.

In the reconstruction of the lineages | have
studied all available material of Recent West
African Terebridae (Bouchet & Le Loeuff, in
prep.). The fauna consists of 17 species, of
which 7 are undescribed; it can be assumed
that this is a reasonable coverage of this tere-
brid fauna. For all species | had specimens
with good protoconchs, thus making the type
of larval development determinable.

It has been demonstrated throughout the
European paleontological literature that the
living representatives of the Miocene and
Pliocene fossils of Europe are to be sought for
on the continental shelf of West Africa. | have

(363)

BOUCHET

FIG. 1. Phyletic relationships of some Neogene Terebridae. Lineage of Terebra senegalensis: 1 Terebra
plicaria, 2 T. modesta, 3 T. fuscata, 4 T. n. sp. and 5 T. senegalensis. Lineage of Terebra (Strioterebrum): 6
Terebra basteroti, 7-8 T. reticulare (7 Pliocene and 8 Recent), 9-10 T. pliocenicum (9 Pliocene and 10
Recent). Lineage of Hastula species: 11 Hastula plicatula, 12 H. striata, 13 H. costulata, 14-15-16 Н. lepida
and its island subspecies; 17 H. subcinerea, 18 H. farinesi, 19 H. exacuminata.

EASTERN ATLANTIC TEREBRIDAE 365

therefore looked for the ancestors of the West
African Recent Terebridae mainly in the trop-
ical/subtropical deposits of the Southern Euro-
pean Neogene. | also reviewed the literature
on the West Atlantic Neogene. The Miocene
and Pliocene Terebridae of Italy have been
the subject of special monographs (Sacco,
1891; Davoli, 1977) and | have studied the
collections of Istituto di Geologia, Torino; Isti-
tuto di Paleontologia, Modena; Institut Royal
des Sciences Naturelles de Belgique, Brus-
sels; Museum National d'Histoire Naturelle,
Paris; and British Museum (Natural History),
London. It has thus been possible to trace
back (with some certainty) the ancestors of
several West African species, and to deter-
mine the type of larval development of each
from juveniles retaining good protoconchs.

DESCRIPTIONS OF THE LINEAGES
1. Lineage of Terebra senegalensis Lamarck

In the Miocene, this lineage starts with
Terebra plicaria Basterot which appears in
the Burdigalian and is widespread in the Hel-
vetian of all southern and central Europe. At
this stage, the shell starts to become more
obtuse, with a shallower suture and less dis-
tinct subsutural groove. It is the form known as
T. modesta Tristan in Defrance, which in the
Tortonian tends to replace Т. plicaria in all of
Europe. The two forms can only be separated
through biometry (Davoli, 1977: 159).

After the Messinian salinity crisis, this line-
age invaded southern Europe once again
probably from populations which had survived
in the Atlantic. This Pliocene form is more
slender than the upper Miocene form, with a
rather indistinct subsutural groove; the axial
ribs are close set on the first teleoconch
whorls and then become more spaced or dis-
appear. This form is called Т. fuscata Brocchi.
The protoconch indicates planktonic larval
development.

After the Pliocene, cold waters replaced the
tropical waters and Т. fuscata migrated
southward to West Africa, invading the con-
tinental shelf south to Angola and the slope of
the oceanic Cape Verde seamounts. The last
event in the lineage is loss of the planktonic
dispersal phase. The Cape Verde populations
have thus become isolated and can today be
regarded as specifically distinct from the con-
tinental populations. The Cape Verde species
(as yet unnamed) is very constant, with a
glossy, pinkish white shell and axial sculpture

present only on the upper whorls. The con-
tinental species, T. senegalensis Lamarck is
more variable in sculpture, with smooth or
ribbed forms although an axial sculpture is
always present on the upper whorls. The shell
is light yellowish brown with a series of sub-
sutural reddish brown spots and sometimes
three series of coloured spiral bands.

2. Lineage of Terebra corrugata Lamarck

This lineage is present in the Neogene of
Europe with a single species, T. acuminata
Borson, which spans the period of the Bur-
digalian to the Pliocene without apparent
change. Its living representative is T. corru-
gata Lamarck which shows the same charac-
ters as the fossil, except that it is more slender
and has a protoconch diameter of 800 um as
compared with 635 шт in lower Pliocene fos-
sils. Both protoconchs are multispiral and of
the planktonic type.

3. Lineage of Terebra (Strioterebrum) species

The Terebra (Strioterebrum) group of spe-
cies is represented in the Miocene of Italy by
three species, of which the type of larval de-
velopment is known for two: T. terebrinum
Bellardi & Michelotti had planktonic larvae,
but did not appear again in the Pliocene after
the Messinian salinity crisis. In the Miocene,
this species was absent from the Atlantic
Portugal and Aquitanian basins and thus
probably became extinct during the drying out
of the Mediterranean. Т. basteroti Nyst also
had planktonic larvae and was common in all
Miocene basins of central and southern Eu-
rope. It gradually evolved into two different
forms, T. reticulare Pecchioli in Sacco with
close-set axial sculpture and strong spiral
lines, and T. pliocenicum Fontannes with
more distant axial ribs and less distinct spi-
rals. Both species retained the planktonic
larvae and have survived in the Recent West
African fauna without significant change.
Recent T. reticulare from the Ivory Coast can-
not be distinguished from Pliocene fossils of
Italy; Recent T. pliocenicum from the same
locality have the axial sculpture a little more
widely spaced than the Pliocene fossils. To-
day they occupy sympatrically two different
niches, T. reticulare on soft muddy sand bot-
toms, while T. pliocenicum favours clean
sand.

The Miocene 7. basteroti stock also prob-
ably at some stage gave rise to four different

366 BOUCHET

FIG. 2. Distribution, adult and larval shells of Tere-
bra fuscata (1), T. senegalensis (2), and T. n. sp.

(3).

recent West African species with direct de-
velopment, but the lack of a fossil record pre-
vents an understanding of this speciation.

4. Lineage of Hastula species

There are four described Recent species of
Hastula in West Africa. Definitely the most
common is H. micans Hinds, characterized by
a very shallow suture and a suprasutural spi-
ral groove. H. micans lives in large numbers
on the wide open sandy beaches with heavy
surf. Surprisingly, no known fossil species can
be regarded as the ancestor of H. micans. It is
possible that this ancestor lived in similar en-
vironment in which it was very unlikely to be-
come fossilized as a fresh, identifiable shell.

А second West African Hastula is H.
knockeri Smith, now restricted to the coasts

FIG. 3. Distribution, adult and larval shells of Tere-
bra acuminata (1) and T. corrugata (2).

of Dahomey and Ivory Coast, and about
which very little is known.

The other two species are more closely re-
lated and apparently shared a common his-
tory back into the Paleogene (H. plicatula
Lamarck). In the Neogene two forms di-
verged: H. striata Basterot and H. sub-
cinerea d’Orbigny; the distinction between
the two forms becomes more obvious in
the mid-Miocene when H. striata evolved
phyletically into H. costulata Borson, with
close-set axial ribs. During this time H. sub-
cinerea evolved into H. farinesi Fontannes
with reduced, widely spaced axial sculp-
ture. The separation of the two species is
complete in the Pliocene. Both H. costulata
and H. farinesi have planktonic larvae.

From the Pliocene H. costulata stock, the
Recent Н. lepida Hinds differs only in having

EASTERN ATLANTIC TEREBRIDAE 367

—

FIG. 4. Distribution, adult and larval shells of Plio-
cene (1) and Recent (2) Terebra reticulare, and of
Pliocene (3) and Recent (4) Т. pliocenicum.

stronger and more widely spaced axial sculp-
ture. However, the larval shell is retained
unchanged as well as the colour marks, still
present on some lower Pliocene shells. The
dispersal capacity of the H. /epida veligers
has enabled it to colonize offshore islands
where subspeciation has occurred: Н. Герда
lepida lives on the shelf of West Africa from
Senegal to Angola while one subspecies (un-
named) is restricted to the Cape Verde Is-
lands and another (unnamed) one lives in the
central and western groups of the Canaries.
The island subspecies differs from the conti-
nental form in being much more slender, with
a smaller aperture, and a dark shell in the
Canarian subspecies. There are more con-
chological differences between the different
subspecies of H. /epida than there are be-

FIG. 5. Distribution, adult and larval shells of Has-
tula costulata (1), H. lepida (2) and its Cape Verde
(3) and Canarian (4) subspecies.

tween H. lepida lepida (Recent) and H. cos-
tulata (lower Pliocene).

The H. subcinerea-farinesi stock was ap-
parently amphiatlantic. Only a few Hastula
taxa have been described in the West Atlantic
Neogene, but forms like H. lissa Jung from the
Miocene of Venezuela are undoubtedly part
of this stock. It is known that Pliocene H.
farinesi had planktonic larvae and probably
the Miocene H. subcinerea-lissa had similar
larval development (it is known for sub-
cinerea) through which genetic exchange
could occur between each side of the Atlantic.
The West African Recent representative of H.
farinesi is H. exacuminata Sacco, which ap-
pears to be a mere local variant of H. salleana
Deshayes, a West Atlantic species with plank-
tonic larvae.

368 BOUCHET

DISCUSSION AND CONCLUSIONS

The main problem in tracing back the origin
of the West African Terebridae in particular,
and of the Recent West African fauna in gen-
eral, is the lack of Neogene deposits along the
whole West African coast. This lack is com-
pensated for by the rich and well studied Mio-
cene and Pliocene fauna of Europe. The
scope of most paleontological studies con-
cerned with this fauna is, however, as stated
in the Introduction, limited to a single horizon
of a particular basin. Considering that these
Neogene deposits have been studied for
more than 150 years, the result is an over-
whelming mass of names. There are more
than 200 specific/subspecific names for the
Neogene Terebridae of Europe while the total
number of species probably did not exceed
25. To some extent it can be said that the
names change with every major geological
stage and with every major basin.

The second problem is the lack of ade-
quately preserved juveniles with protoconchs.
This is the primary reason in this paper for
lack of information on several Miocene Tere-
bridae; the type of larval development is
known for most Pliocene species.

It is difficult to compare the results obtained
on the evolution of protoconchs with other
similar results because they are few and con-
cern prosobranch groups that are only dis-
tantly related to Terebridae.

Smith (1945) has shown in West Atlantic
Ficus (Ficidae) a phyletic evolution from
forms with planktonic larvae in the lower Mio-
cene to forms with direct development in the
Recent. Gougerot & Le Renard (1980) have
shown from protoconch observations an evo-
lution from planktonic to lecithotrophic type of
development in Triforis bitubulatus Baudon
(Triforidae) in the Eocene of the Paris basin. A
similar type of evolution is shown here in the
Terebra senegalensis lineage.

Robertson (1973) remarked that “in the
evolution of Philippia (Architectonicidae)
there are indications that protoconch size and
morphology are among the first characters to
change” and showed protoconch enlarge-
ment in the Cenozoic evolution of the genus.
At the species level, this compares with the
evolution described here for the Тегебга
acuminata-corrugata series.

The case of the Hastula lineage is interest-
ing because it suggests that the rate of ap-
pearance or extinction of characters may dif-
fer between species stemming from a com-
mon ancestor and sharing the same type of

larval development. Geographical isolation
seems to act more rapidly than the phyletic
change of Hastula costulata-lepida over the
whole Pliocene.

More generally, we can now turn back to
the questions asked by Scheltema (1977b):

What evidence from the fossil records
supports the notion that dispersal capability
is related to species temporal longevity?

Hansen (1980) and Shuto (1974) have
published data on the evolution of Volutacea
and Buccinacea, but | think one should be
very careful to avoid circular reasoning in the
answer to this question. This answer depends
on the species concept in a phyletic lineage.
When one deals with species with planktonic
larvae, one assumes that dispersal is linked
with the capacity for a species to become
adapted to broad latitudinal and hydrological
conditions. Thus an interpopulation variability
is interpreted in terms of phenotypical varia-
tion. With this in mind, time changes in a line-
age will similarly be interpreted as of infraspe-
cific rank.

When considering species with direct de-
velopment, interpopulation variability is inter-
preted in connection with the absence of
genetic exchange through the larval life. Het-
erogeneity is interpreted as being genetically
determined and thus different morphs along a
continuum (geographical or chronal) are fre-
quently given specific rank.

However, the example of Recent species
shows that the Arctic shallow water gastro-
pods, which all have direct development,
have huge intraspecific variability. Many
temperate/tropical species with planktonic
larvae have interspecific differences which in
paleontology would frequently be interpreted
as infraspecific variability.

What evidence supports the idea that al-
lopatric speciation is connected with mode of
reproduction and dispersal capability?

The results of this study on Terebridae can
be classified into three degrees of speciation
since the lower Pliocene:

1. No speciation or phyletic subspeciation:
Terebra acuminata-corrugata (planktonic); T.
reticulare (planktonic) and 7. pliocenicum
(planktonic); Hastula farinesi-salleana (plank-
tonic).

2. No speciation over time; allopatric sub-
speciaton in Recent: H. costulata-lepida
(planktonic).

3. Speciation through time and space: T.
fuscata (planktonic)-senegalensis (direct)-
n.sp. (direct).

Thus this limited evidence supports the

EASTERN ATLANTIC TEREBRIDAE 369

idea that allopatric speciation is connected
with nonplanktonic larval development. But
the study of many additional lineages is
needed to provide a more statistical answer.
In this respect the Neogene of Europe can
offer a rich fauna which is reasonably well de-
scribed, together with good paleogeographic
and stratigraphical data.

ACKNOWLEDGEMENTS

| thank especially Dr. G. Pavia (Torino) and
Dr. F. Davoli (Modena) who put their collec-
tions of respectively Pliocene and Miocene
Terebridae at my disposal. | am also grateful
to the curators of paleontology of the Institut
Royal des Sciences Naturelles (IRSN, Dr. A.
DHondt), British Museum (Dr. N. Morris) and
Museum National d’Histoire Naturelle (Dr. J.
C. Fischer). The drawings of protoconchs
have been prepared by Ms. C. Beauchamp
and the photos by Mr. A. Foubert.

REFERENCES CITED

DAVOLI, F., 1977, Terebridae (Gastropoda). In
Montanaro Gallitelli, E. (ed.), Studi monografici
sulla malacologia miocenica modenese. Parte |.
| Molluschi tortoniani di Montegibbio. Paleonto-
graphica ltalica, 70: 135-169, pl. 17-20.

GOUGEROT, |. & LE RENARD, J., 1980, Clefs de
détermination des petites espèces de Gastéro-
podes de ГЕосепе du bassin parisien. XII. La
famille des Triphoridae. Cahiers des Natural-
istes, 35: 41-59.

HANSEN, Т. A., 1980, Influence of larval dispersal
and geographic distribution on species longevity
in neogastropods. Paleobiology, 6: 193-207.

ROBERTSON, R., 1964, Dispersal and wastage of
larval Philippia , krebsii т the North Atlantic.
Proceedings of the Academy of Natural Sci-
ences of Philadelphia, 116: 1-27.

ROBERTSON, R., 1973, On the fossil history and
intrageneric relationships of Philippia. Proceed-
ings of the Academy of Natural Sciences of
Philadelphia, 125: 37-46.

ROBERTSON, R., 1976, Marine Prosobranch
Gastropods: Larval studies and systematics.
Thalassia Jugoslavica, 10: 213-238.

SACCO, F., 1891, | Molluschi dei terreni terziarii del
Piemonte e della Liguria. Parte X: Cassididae
(aggiunte), Terebridae e Pusionellidae. Clausen,
Torino, 66 p., 2 pl.

SCHELTEMA, R. S., 1966, Evidence for trans-
Atlantic transport of gastropod larvae belonging
to the genus Cymatium. Deep Sea Research,
13: 83-95.

SCHELTEMA, В. S., 1971, Larval dispersal as а
means of genetic exchange between geographi-
cally separated populations of shallow-water
benthic marine gastropods. Biological Bulletin,
140: 284-322.

SCHELTEMA, R. S., 1972, Dispersal of larvae as a
means of genetic exchange between widely
separated populations of shoalwater benthic in-
vertebrate species. п BATTAGLIA , B., ed., Fifth
European Marine Biological Symposium, Piccin,
Padova, p. 101-114.

SCHELTEMA, В. S., 1977a, Dispersal of marine
invertebrate organisms: paleobiogeographic and
biostratigraphic implications. KAUFFMAN, E. G.
& HAZEL, J. E. (eds.), Concepts and Methods
of Biostratigraphy. Dowden, Hutchison and
Ross, Stroudsburg, р. 73-108.

SCHELTEMA, R. S., 1977b, On the relationship be-
tween dispersal of pelagic veliger larvae and the
evolution of marine prosobranch gastropods. In
BATTAGLIA, B. & BEARDMORE, J. (eds.),
Marine Organisms. Plenum, New York, р. 303-
322.

SHUTO, T., 1974, Larval ecology of prosobranch
gastropods and its bearing on biogeography and
paleontology. Lethaia, 7: 239-256.

SMITH, B., 1945, Observations on gastropod pro-
toconchs. Paleontographica Americana, 3(19):
1-48, pl. 21-23.

THORSON, G., 1946, Reproduction and larval de-
velopment of Danish marine bottom Inverte-
brates, with special reference to the planktonic
larvae in the Sound. Meddelelser fra Kommis-
sionen for Danmarks Fiskeri- og Havunder-
sggelser, serie Plankton, 4(1): 1-523.

THORSON, G., 1961, Length of pelagic larval life in
marine bottom Invertebrates as related to larval
transport by ocean currents. Publications of the
American Association for the Advancement of
Science, 67: 455474.

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MALACOLOGIA, 1981, 21(1-2): 371—401

THE MOLLUSCAN DIGESTIVE SYSTEM IN EVOLUTION

Luitfried v. Salvini-Plawen

Institut für Zoologie, Universitat Wien, Dr. Karl Lueger-Ring 1, A1010 Wien |, Austria

ABSTRACT

A comparative analysis of molluscan alimentary conditions including anatomy, way of life, and
digestive as well as feeding properties dependent on diets is given with special attention to
conditions in the Caudofoveata and Solenogastres which have hardly been considered until
now. Such outlines reveal that the original diets of the ancestral molluscs consisted of micro-
organisms and/or deposit matter in general, taken up from a fairly firm substratum by means of a
broad monoserial radula. The (presumably) initial, intracellular as well as extracellular digestion
later on convergently selected the separation of a midgut gland off the straight alimentary
canal—single in Caudofoveata, and paired in Placophora-Conchifera—serving for pure secre-
tion (Caudofoveata; Bivalvia-Nuculidae) and even as the restricted site of actual digestion.
Further adaptation included the differentiation of a food-mucus column or protostyle in at least
two evolutionary lines (Caudofoveata; Conchifera), of a diphyletic gastric shield, and even of a
true crystalline style (Tryblidiida, Gastropoda, Bivalvia). Also the chitinous, so-called peritrophic
membrane is no monophyletic character. Other, i.e. mostly macrovorous, food taken up pre-
dominantly in a predaceous (carnivorous) way does not include such strictly correlated at-
tributes, with the exception of respective pharyngeal conditions (radula; seizing/sucking/swal-
lowing mechanisms, etc.) and of a fairly short alimentary canal (Solenogastres, Scaphopoda,
Cephalopoda in general; Gastropoda-Heteropoda, -Neogastropoda, etc.).

Such knowledge facilitates the understanding of selective pressures responsible for supra-
specific evolution and enables us to accept 1. an unspecialized microvorous diet on marine
deposits as a key character for the Caudofoveata to burrow in soft sediments (subsequently
causing other adaptive reorganization: pedal shield, worm-like shape, etc.); 2. a microherbi-
vorous diet on hard bottoms as a key character for special adaptations in the Placophora
(esophageal and midgut glands, slender intestine; subradular organ); 3. primitive placophoran
conditions also principally existing congenitally in ancestral Conchifera (= Galeroconcha), within
which the unselective deposit-feeding may have essentially contributed to the survival of direct
descendents: Tryblidiida; 4. microvorous diet also as original (and in part highly specialized) in
two of the Galeroconcha offspring, the Gastropoda and the Bivalvia, whereas other descendent
groups originated by assuming different diets, such as micro-carnivory in Scaphopoda and the
swailowing of carrion to predatory feeding in Cephalopoda; 5. an early alteration from micro-
vorous to Cnidaria-vorous feeding as a key character for the Solenogastres, inducing respective
behavioural adaptation in locomotion and therefore narrowing the body shape (followed by other
organizational consequences: internalization of the posteriorly limited mantle grooves, regres-
sion of gonoducts, etc.). Thus, in avoidance of those adaptations to microvorous feeding (midgut
gland, protostyle, gastric shield, etc.), the Solenogastres evidently retained the most conserva-
tive configuration of the digestive system in general within the Mollusca.

INTRODUCTION

Comparative analyses of various kinds
within animal groups have frequently been
based upon information gained only from
familiar and quantitatively important sub-
groups, thus neglecting ones which are less
familiar but of equal qualitative importance.
Such a biased representation often also con-

cerns the Mollusca, frequently resulting in
misleading conclusions especially with regard
to primitive conditions of the phylum as a
whole.

Increased knowledge and more compre-
hensive analyses have revealed that the an-
cestral patterns of molluscs are more closely
retained in the still shell-less Caudofoveata
and Solenogastres,! the synorganization of

1Because of the characters of the mantle and the gonopericardial system, both classes have formerly been classified as
Chaetodermatina, etc., and as solenogastrid Neomeniina, etc., within a single taxon Aplacophora. Since such an assem-
blage (cf. Scheltema, 1978) negates their evolutionary diphyletic origin and artificially unites two basically independent lines
(cf. S. Hoffman, 1949, and others), the Chaetodermatina had been separated from the solenogastrid aplacophorans as a
proper class Caudofoveata (cf. Salvini-Plawen, 1969a, 1972c, 1980).

(371)

372 SALVINI-PLAWEN

their characters is evidenced to be more con-
servative than that of Neopilina, for example
(cf. Vagvolgyi, 1967; Degens et al., 1967;
Salvini-Plawen, 1969a, 1972c, 1980, 1981;
Peters, 1972; Stasek, 1972; Trueman, 1976).
An extensive consideration of molluscan or-
ganization in respect to the comparative rep-
resentation of groups being of equivalent evo-
lutionary levels must also include alimentary
conditions (cf. Graham, 1955). In conformity
with this purpose, equivalent emphasis
should be placed on those minor groups
which are not ordinarily discussed because of
lack of familiarity or knowledge. Conclusions
tracing anagenetic and primitive molluscan
patterns onto the already highly developed
Gastropoda and Bivalvia only (cf. Graham,
1949; Owen, 1966a, b) must lead to misinter-
pretation. ;

An analysis of digestive and feeding prop-
erties dependent on diets may not only eluci-
date specific morphological and physiological
conditions, but may well contribute to our
knowledge of phyletic trends with respect to
behavioural adaptations. Since most organ
systems are dependent on each other (form-
function complex, cf. Bock & Wahlert, 1965),
evolutionary pathways can largely be ex-
plained by synorganized alterations predomi-
nantly following selection pressure for food,
habitat, and mode of locomotion (cf. Mayr,
1970). An accurate scrutiny of the alimentary
conditions may thus essentially facilitate the
understanding of selective pressures respon-
sible for supraspecific evolution.

A) MOLLUSCAN ALIMENTARY
CONDITIONS

Information on feeding, anatomical, and di-
gestive properties is fairly detailed as con-
cerns the major groups of gastropods, bi-
valves, and siphonopods (cephalopods). In
the attempt to come to an equivalent basis for
all classes with respect to a comparative esti-
mation of the alimentary conditions, special
attention is paid to—and a more detailed ac-
count is given for—those groups which so far
have not been treated.

1. Caudofoveata

The Caudofoveata are still shell-less (apla-
cophorous), vermiform molluscs of 2 to
140 mm in length, and their mantle is covered
by a chitinous cuticle as well as by aragonitic
scales and terminal spines; the lateral mantle
edges are fused midventrally and the ventral
gliding surface is merely characterized by its
cerebrally innervated, post- or perioral rudi-
ment, the pedal shield (evolutionary line of
Scutopoda; cf. Salvini-Plawen, 1980). The
mantle cavity is in a terminal position and con-
tains one pair of ctenidia. The radula is disti-
chous, the alimentary tract straight, and the
midgut exhibits posteriorly a narrow intestine
and a voluminous ventral midgut sac. The
sexes are separate, the conveyence of the
sexual products occurs via pericardioducts;
fertilization is external. The animals are

FIG. 1 Caudofoveata: radular sheath of Scutopus ventrolineatus; A, in anterior cross section; B, in longitu-
dinal section; C, in posterior cross section. bm = radular membrane (ribbon), od = odontoblasts.

MOLLUSCAN DIGESTIVE SYSTEMS 373

marine burrowers of muddy sediments, feed-
ing On microorganisms and organic matter.
There are 66 species in three families.
Digestive system: The digestive system in
Caudofoveata begins with a mouth opening
surrounded by a distinct muscular sphincter; it
leads into the folded, expandible and protru-
sile buccal cavity provided with some glandu-
lar cells. The preradular foregut is cuticular-
ized, or only ciliated in Chaetodermatidae, and
there are three sets of predominantly follicular
glands: (1) Some unicellular ventral glands
just in front of the radula opening on a small
papilla (“subradular organ” of Heath; cf.
Schwabl, 1963: 261); (2) a pair of lobular
lateral organs close to the radula (Chaeto-
dermatidae only ?); (3) a mass of dorsal
glands above the radula or some distance
behind, primitively being epithelial, otherwise
but subepithelial follicles in a paired arrange-
ment (Scutopus robustus, Chaetodermati-
dae) which may be correlated with a proper
dorsal pouch. In Prochaetoderma a pair of
chitinized, spatulate and large cuticular ele-
ments ("mandibles”) are differentiated in ob-
lique position each in a voluminous lateral fore-
gut pouch. Psilodens lacks a subradular sac.
The radulae of all Caudofoveata are dis-
tichous, viz. two erected curved teeth per row2
are differentiated upon a true radular mem-
brane or ribbon (Scutopus, Limifossor,
Prochaetoderma; see Fig. 1), proximally
underlain by the pharyngeal subradular mem-
brane (cf. also Scheltema, 1978); additionally,
in Prochaetoderma the sheath produces
lateral alate structures. The elaboration of the
radula apparatus (denticulation, alae, and
supportive elements) is important for the clas-
sification’ at the family level (Salvini-Plawen,
1969b, 1975), but exhibits in all members ex-
cept the Chaetodermatidae a basically typical
fashion. In the latter, however, there is only
one transverse row of teeth which in Chaeto-
derma is reduced to a pair of simple denticles
or is even totally lost. In compensation, the
radular membrane is elaborated to form a
large conical element (basal plate or cone)
associated with one or two pairs of cuticular
lateral supports and some smaller elements
(cf. Scheltema, 1972; Salvini-Plawen & Nopp,
1974). The typical radula of the more con-
servative caudofoveates is characteristically

developed within its sheath by distal odonto-
blasts (Fig. 1), the lower/anterior of which
secrete the ribbon and the upper/terminal
ones produce the teeth themselves; the
dorsal epithelium contributes by hardening
the distal portion of the teeth (sclerotization).
In Chaetodermatidae the sheath is replaced
by a small radular pit and the subsequent
tongue-like, cone-producing pouch. In all
members a well defined pair of bolsters of
muscular as well as connective tissue, and
frequently also turgescent cells support the
radula. A generically different system of 8-13
muscle groups is associated with the radula
apparatus, 6-8 of which can be homologized
throughout (K. Deimel, 1981, Diss. Univ. Wien).

The postradular (esophageal) foregut gen-
erally shows some ciliated areas, and its
Opening into the midgut may be equipped with
a sphincter. As in the case of the radula ap-
paratus, new investigations demonstrate that
the differentiation of the midgut approximately
reflects gradual properties at the family level:
the more primitive condition is represented in
Psilodens (P. elongatus) and Metachaeto-
derma, both of which possess an extended,
somewhat pouched midgut, ventrally and
laterally lined by the large inflated cells with a
voluminous glandular body escaping into the
gut lumen after rupture of the cell wall (‘club-
shaped’ cells or ‘Keulenzellen’; Fig. 2). Dor-
sally the midgut is provided with a simple,
cubical epithelium of indifferent appearance,
whereas at the rims of the intruding folds,
cells varying in shape from cylindrical to club-
shaped can be seen to be densely packed
with coarse granula (‘granula-cells’ ог
‘KOrnerzellen’; Fig. 2); the distal portion of the
cells are apocrinely cast off to be mixed with
the food particles. The histological differentia-
tion can be pursued further to the single, vol-
uminous midgut sac or gland which is ventral-
ly separated from the posterior midgut (or in-
testine) not before the midbody; the granula-
cells are here arranged more broadly beneath
the gonad(s) extending dorsally or somewhat
laterodorsally. The ciliated intestine is straight
and narrow, but very extensible. It begins
laterodorsally together with the midgut sac,
the transitional region to the former is likewise
ciliated, and it leads directly to the mantle
Cavity.

2The former statement of five elements per transverse row (as recently also accepted by Ivanov, 1979: 9) is due to a

misinterpretation of cuticular and ribbon elements.

Ivanov's classification (1979) cannot be accepted since it is based upon misinterpretations noted above (footnote 2).

374 SALVINI-PLAWEN

FIG. 2. Caudofoveata: dorsolateral detail of cross
section through the midgut sac of Chaetoderma
nitidulum. dc = club-shaped cells, дс = granula-
cells.

OY,

A
D

Г.
[=

Ce}

Other limifossorids (Scutopus, Limifossor)
possess a comparatively short, pouched mid-
gut lined by an epithelium cubical to columnar
in shape and filled with fine granula. The ter-
minal area (with the emergence of the intes-
tine) is also ciliated, but the ‘granula-cells’ and
‘club-shaped’ cells are here confined (with
identical arrangement) solely to the midgut
sac (Fig. 3A) which is already separated in the
anterior third of the body. In both described
species of Prochaetoderma, the short midgut
is subdivided histologically into an anterior-
dorsal lining of more or less cubical cells with
fine granulation and into a posterior-ventral
area consisting of densely granulated cells
similar to the ‘granula-cells’ of the midgut
gland in other species. The latter organ in
Prochaetoderma is considerably lobulated
and lined by one kind of cell appearing to be a
modified ‘club-shaped’ type.

With the exception of Falcidens crossotus,
all Chaetodermatidae so far investigated
show a distinct separation of the short midgut
with cubical, finely granulated cells, and a
midgut sac with typical ‘club-shaped’ cells as
well as latero-dorsal ‘granula-cells’ (Figs. 2,
3B); in F. crossotus most of the lining in the
midgut gland is made up of ‘granula-cells’
and the arrangement of the ‘club-shaped’
cells is confined to a ventral band. In all these

FIG. 3. Caudofoveata: cross section through separation of the midgut sac from the midgut proper, A in
Scutopus ventrolineatus (Limifossoridae) just after separation, B in Falcidens aequabilis (Chaetodermati-
dae) with gastric shield. ao = aorta, dc = club-shaped cell and gc = granula-cell of midgut sac, gs = gastric

shield.

MOLLUSCAN DIGESTIVE SYSTEMS 375

Chaetodermatidae, however (F. hartmani, F.
crossotus, F. gutturosus, F. caudatus, F.
aequabilis; Chaetoderma nitidulum, С.
canadense, C. intermedium, C. recisum, C.
rectum), the midgut itself differentiates to-
wards a stomach; at its terminal, ciliated sec-
tion an area close to the entrance into the
intestine consists of a cuticular cover with a
medially knob-like rim (tooth); this cuticular-
ized area constitutes a primitive gastric shield
not present in other Caudofoveata (Fig. 3; see
below, also Scheltema, 1978).

Diets: As far as the present information
reveals (Table 1), there is surprising homo-
geneity in the general food of Caudofoveata.
In all species examined, the diets consist of
microorganisms and/or organic detritus when
inferred from gut contents. There are, how-
ever, no direct observations on feeding and
only the exceptional observations on
Prochaetoderma (see below) as well as the
conditions in Chaetoderma eruditum (cf.
Heath, 1904) or in Falcidens caudatus (Table
1) reflect indirectly on the food itself. This in-
sight as well as some striking differences in
the amount of the respective food remnants in
the gut point to the evidence that several spe-
cies might take up their food selectively (e.g.
C. montereyense). On the other hand, owing
to the lack of direct observations, we do not
know about diets which undergo total solution
without leaving recognizable remains in the
gut. We may also point to the establishment of
cuticular skeletons obviously coming from
entomostracans (Scutopus ventrolineatus,
Prochaetoderma californicum, Falcidens
crossotus, Е. gutturosus, Е. aequabilis,
Chaetoderma canadense, C. eruditum); like
those, some other specific food is well imagin-
able. In accordance with the burrowing man-
ner of living, all diets come from the marine
bottom-layer; findings of other particles and/
or stated organisms, therefore, may be an ac-
cidental by-product.

The most surprising condition is met with
regard to the radula. Though they possess
typical distichous teeth in several transverse
rows, the more conservative Limifossoridae
and Prochaetoderma obviously do not essen-
tially differ in their diets from the highly speci-
alized Chaetodermatidae (see below). Since
we may consider the chaetodermatid radula
as an adaptation for the uptake of food, the
distichous and partially hooked radula of the
more primitive members does not conceivably
appear to be a primary adjustment for a simi-
lar microphagous diet; present data, however,

do not allow any other conclusions. Surveying
the food-relations of the Caudofoveata, there
is clear evidence that most if not all Recent
members of the group feed on microorgan-
isms and/or deposit matter in general; no
principal difference can be seen with respect
to the more conservative representatives
possessing an allegedly predatory type of
radula.

Feeding mechanisms and digestion:
Owing to their concealed manner of life, there
are few observations on the food uptake of
burrowing Caudofoveata. Kowalevsky (1901:
280-281) reports for Prochaetoderma radu-
liferum that the radula is projected and con-
tinuously moves both rows of teeth against
each other as if they were searching for some
objects to be pushed into the buccal cavity.
Nearly identical observations have been
made by the present author on the same spe-
cies: obviously to gather food, the perioral por-
tion of the body becomes shortened and the
pharyngeal spatulae (so-called mandibles)
spread wide to support it. Simultaneously the
radula protrudes and is displayed in order to
brush and rake in food particles. Both these
observations coincide with the function of the
radula, i.e. to brush and seize sediment parti-
cles without specific selection. Similar action
of the radula apparatus is described by Heath
(1905: 714-715) for Limifossor talpoideus,
although the spread radula itself seems not
to be actually protruded out of the mouth
opening. There is no further direct evidence
on feeding mechanisms. Concerning the
Chaetodermatidae with their strongly altered
radula apparatus, Heath (1904: 460; 1911:
25) presumes an active food-gathering func-
tion of the pedal shield for Chaetoderma; this
would also correspond to the anatomical con-
dition (musculature, etc.) that the radula here
is apparently not brought to the tip of the fore-
gut. Problems arise, however, concerning the
function of the radula т Falcidens, where the
two single, forcep-like teeth appear pre-
destined to seize objects; the respective
musculature and the findings in F. caudatus
(Table 1) concur with that hypothesis, which
also would infer radular manipulation of select-
ed food (see above).

The food taken up is carried backwards
(presumably) by means of the radula (Heath,
1905) or the chaetodermatid basal cone re-
spectively (Heath, 1911). After being broken
up by the enzymatic secretion of the foregut
glands, the food is passed through the post-
radular foregut by muscular action supported

376

TABLE 1. Diets in Caudofoveata.

SALVINI-PLAWEN

Species

Contents of gut or faecal pellets

Reference

LIMIFOSSORIDAE

Scutopus ventrolineatus
Salvini-Plawen

Scutopus robustus
Salvini-Plawen

Limifossor talpoideus
Heath

Psilodens elongatus
(Salvini-Plawen)

PROCHAETODERMATIDAE
Prochaetoderma raduliferum
(Kowalevsky)

Prochaetoderma californicum
Schwabl

CHAETODERMATIDAE
Falcidens gutturosus
(Kowalevsky)

Falcidens crossotus
Salvini-Plawen

Falcidens caudatus
(Heath)

Falcidens aequabilis
Salvini-Plawen

Chaetoderma nitidulum
Loven

Chaetoderma canadense
Nierstrasz

Chaetoderma eruditum
Heath

Chaetoderma hawaiiense
Heath

Chaetoderma montereyense
Heath

Chaetoderma argenteum
Heath

Chaetoderma californicum
Heath

Chaetoderma nanulum
Heath

Chaetoderma japonicum
Heath

Chaetoderma bacillum
Heath

Chaetoderma squamosum
Heath

organic debris (minute fragments of tests,
spicules, cuticular skeletons)

granular coagulum with some debris

granular coagulum with some diatoms,
sponge spicules, inorganic debris
organic debris (minute skeletal fragments)

organic and inorganic debris; one intact
turret-like foraminifer
(230 um x 200 ит)

fragments of radiolaria, diatoms, spicules;
crustacean eggs; cuticular skeletons

diatoms, fragments of radiolaria, sponge
spicules, cuticular skeletons; organic
debris

fragments of arthropod legs and other
cuticular skeletons, sponge spicules;
organic and inorganic debris; em-
bedded protist parasites

one specimen with 5 intact Foraminifera-
Textularia (300 um-600 um) in the
foregut

organic debris with a few cuticular struc-
tures, diatoms, and some inorganic
matter

tests of diatoms, foraminifers, some
radiolaria; organic and inorganic debris

fragments of cuticular skeletons and
sponge spicules, organic and inor-
ganic debris

organic debris with bits of plants, vegeta-
ble spores, foraminifers, sponge spic-
ules; intact Foraminifera-Rotalia; di-
atoms, fragments of entomostracans

diatoms, plant spores, sponge spicules,
organic debris

diatoms; organic and inorganic debris

radiolaria, diatoms, sponge spicules, or-
ganic and inorganic debris; embedded
protist parasites

fragments of radiolaria and sponge
spicules, organic debris

diatoms, sponge spicules

diatoms, organic and inorganic debris

diatoms, sponge spicules, inorganic
debris

Salvini-Plawen (unpubl.)
Salvini-Plawen (unpubl.)
Heath, 1905, 1911
Salvini-Plawen (unpubl.)
Kowalevsky, 1901;
Salvini-Plawen (unpubl.)

Schwabl & Salvini-Plawen
(unpubl.)

Salvini-Plawen (unpubl.)

Wirén, 1892; Salvini-
Plawen (unpubl.)
Salvini-Plawen (unpubl.)

Heath, 1904, 1911

Heath, 1911
Heath, 1911
Heath, 1911

Heath, 1911

Heath, 1911
Heath, 1911
Heath, 1918

Heath, 1918

MOLLUSCAN DIGESTIVE SYSTEMS 377

TABLE 1. (Continued)
Species

Chaetoderma intermedium
Knipowitsch

Contents of gut or faecal pellets

granular coagulum mainly with inorganic
debris, a few sponge spicules and frag-

Reference

Salvini-Plawen (unpubl.)

ments of radiolaria

Chaetoderma (?) militare

Selenka spicules

by ciliated areas (when present); there it is
mixed with the secretions of the dorsal glands
to become a mucous bolus or strand contain-
ing the particles (the mucus string is, how-
ever, produced even when food material is
absent). The midgut is the principal site of di-
gestion which obviously takes place entirely
extracellularly—although pinocytosis may oc-
cur (compare Owen, 1966b: 65f). Commonly
a greater number of the large bodies of the
“club-shaped' cells in the midgut sac is found in
the lumen where they undergo slow solution;
but they are occasionally found even still in
the faeces. The released contents of the
apocrine portion of the ‘granula-cells’ are also
found and undergo disintegration. At least in
some species (Scutopus ventrolineatus,
Falcidens aequabilis, Е. crossotus, F.
liosquameus), food particles bound by the
mucus strand are conveyed through the gut
by middorsal cilia; they are mixed with the
digestive secretions and compacted in the
posterior region to a food-mucus column
which, in accordance with the arrangement of
its components, is rotated there by the cilia
usually present. In more conservative mem-
bers such as Scutopus and also Prochaeto-
derma, the mucous food strand is continuous
directly into the intestine, at the beginning of
which it is divided into pellets. In the chaeto-
dermatids (so far as investigated) there is a
primitive gastric shield including a “tooth”
(see above), and the compacted food column
with a central mucus rod and peripherally
bound particles correspond to an ergatulum
or protostyle (cf. Owen, 1966b: 61 f). The
faecal pellets are conveyed in the long, ciliat-
ed intestine and are generally ovoid in form;
they measure in Falcidens crossotus up to
300 ит x 80 ит. They contain food rem-
nants and frequently a portion of the mucus
column, too; the latter are in F. crossotus up
to 185 um x 40 um, and even up to
230 um x 40 ит т Scutopus robustus.
Each pellet is enciosed т a so-called peritro-
phic membrane which, as in F. aequabilis,

fragments of radiolaria, diatoms, sponge

Salvini-Plawen (unpubl.)

may be continuous to form a string of pellets;
as identified in Scutopus ventrolineatus,
Falcidens gutturosus, and Chaetoderma
canadense, that peritrophic membrane is
produced in the midgut proper.

2. Solenogastres

The Solenogastres are still shell-less
(aplacophorous), laterally narrowed molluscs
of 1 mm to 300 mm in length, and their mantle
is covered by a chitinous cuticle and aragoni-
tic scales or spicules; the foot is narrowed to a
groove usually provided with longitudinal folds
and begins with a distinct pedal gland (line of
Adenopoda; cf. Salvini-Plawen, 1972c, 1980).
The subterminal mantle cavity bears no
ctenidia but is often equipped with secondary
respiratory formations (plicae, papillae)—the
anterolateral sections of the mantle cavity are
reduced and the posterolateral ones are in-
ternalized. The straight midgut shows serial
lateroventral expansions. The animals are
hermaphroditic, the gonoducts are usually
reduced and the conveyance of the sexual
products then occurs via the pericardioducts;
there is internal fertilization, and there are
accessory genital organs. The animals are
marine, mostly cnidariavorous epibionts.
There are 180 species in four orders.

Digestive system: The digestive system
in Solenogastres appears to be exceptional
because it possesses no separate midgut
gland, and also has not developed a radular
ribbon; both characters, however, can be
judged primitive (see below). The mouth
opening and/or buccal cavity is located be-
hind or dorsoposteriorly within the atrial sense
organ (the remnant of the preoral mantle cavi-
ty; cf. S. Hoffman, 1949). It leads into a gen-
erally expandible and cuticularized foregut. In
its preradular portion, this tube is often pro-
vided with an initial sphincter and other dis-
tinct musculature, thus representing a pharynx
frequently functioning as a suction pump

378 SALVINI-PLAWEN

(Salvini-Plawen, 1967b). When present, a dis-
tinct postradular foregut or esophagus serves
predominantly a glandular secretive function.
Within the Solenogastres four principal sets of
foregut glands can be distinguished (cf.
Salvini-Plawen, 1978): (1) single subepithelial
pharyngeal glands; (2) a distinct dorso-
pharyngeal follicle gland; (3) one pair of
(ventral) glandular organs, the ducts of which
generally open lateroventral to the radula ap-
paratus; (4) single subepithelial esophageal
glands. Either the pharyngeal glands (1) or
the tubular organs (3) are obligately present
and only occasionally substituted by special
formations. Most important for classification at
the family level, the lateroventral tubular
organs (3) in their turn are differentiated in
four different types (Salvini-Plawen, 1967b,
1972a, 1978).

The radula apparatus consists of a highly
variable radula itself with different numbers of
transverse rows, which in general rest upon a
direct continuation of the pharyngeal cuticle,
the basal cuticle (compare the subradular
membrane in other molluscs). A radula bol-
ster may be represented merely by a simple
accumulation of muscular and connective tis-
sue forming a median or paired support. More
specialized degrees exhibit a distinct muscu-
lar concentration sometimes even provided
with turgescent cells. Though only rarely ob-
served in the living state, the radula may fre-
quently be protruded towards the mouth due
to associated, distinct pro- and retractors. The
radula itself is produced as usual in a separate
sheath by odontoblasts, and the dorsal epi-

A B

cut

thelium of the sheath contributes to the
sclerotization of the teeth (compare Fig. 5).
Worn-out teeth are cast off, or retained
throughout life in the continuously growing
ventral radula sac(s). The shape of the teeth
may be categorized in four types of taxonomic
value at the family level: (1) monoserial plates
with varying denticulation; (2) biserial, serrate
plates; (3) biserial, erected teeth with median
hooks (distichous type); (4) numerous teeth

FIG. 4. Solenogastres: morphogenesis of the dis-
tichous radula of Pruvotina impexa (from Salvini-
Plawen, 1972c).

100 u

FIG. 5. Solenogastres: morphogenesis of the biserial radula of Simrothiella schizoradulata (from Salvini-
Plawen, 1978). A, a pair of still medially joined plates enclosed in the sheath; B, separation in the junction of
sheath and foregut; C, radula exposed in the pharynx. Black areas are sclerotized. cut = basal cuticle.

MOLLUSCAN DIGESTIVE SYSTEMS 379

per transverse row (polyserial and polystich-
Ous types). As concern the presumably primi-
tive type of solenogastrid radula, distinct evi-
dence is found that the biserial and distichous
types are derived from the monoserial radula:
Figs. 4 and 5 (cf. Salvini-Plawen, 1972c,
1978); the polyserial/polystichous radula
being already differentiated only within more
specialized families. In different independent
evolutionary lines, the radula has been re-
duced, mostly in connection with sucking up
food.

The midgut is generally sharply separated
from the foregut, while the latter is often addi-
tionally provided with a terminal sphincter.
The midgut occupies the whole body cavity
with the exception of the middorsal and mid-
ventral spaces (dorsal gonads, ventral-sinus);
there is often the differentiation of a distinct
frontal caecum. Owing to the random serial
arrangement of the dorsoventral pair of mus-
cle bundles, the midgut generally exhibits a
lateroventrally pouched configuration; т
some species (especially very small ones) no
pouches are present, since the serial dorso-
ventral musculature runs alongside the body
wall. The midgut is lined by a high, glandular
digestive and resorptive epithelium of club-
shaped cells with enzymatic granula and
bodies; sometimes two different types of cells
have been reported which, however, may be
due to varying developmental stages. Gen-
erally, a middorsal ciliated strip or fold is pres-
ent; this continues into the short, ciliated
rectum which opens dorsally into the mantle
Cavity.

Diets: Up to the last decade little was
known about diets in the Solenogastres; in-
formation on the contents of the gut as well as
inferences of epizoic condition were sum-
marized in Hoffmann (1930), Graham (1955),
and Hyman (1967). Recent investigations,
however, resulted in the identification of
numerous relations to the food sources sum-
marized in Table 2. This list clearly demon-
strates that most Solenogastres are depend-
ent on Cnidaria as a food source, the special-
ization to which is demonstrated by the
Solenogastres' ability to prevent the explosion
of nematocysts (Salvini-Plawen, 1967a,
1968). These are obviously embedded within
mucous secretions and taken up in an unex-
ploded condition (Salvini-Plawen, 1972b);
Moreover, they remain intact and are able to
retain their ability to explode (Salvini-Plawen,
1968).

There are a few Solenogastres with diets

other than Cnidaria. Setting aside occasional
cases of uptake of diatoms, etc. as well as of
Organic debris (see Micromenia fodiens,
Nematomenia tengulata, | Archaeomenia
prisca, Hemeimenia intermedia, also Pro-
neomenia sluiteri and others), only Dorymenia
usarpi may actually feed on microorganisms
by brushing the surface of the sediment with its
radula (although one specimen has been re-
corded in an epizoic condition). A somewhat
enigmatic condition is found in Anamenia
gorgonophila, Proneomenia sluiteri, and
Rhipidoherpia copulobursata, in which
arthropods (entomostracans) have been re-
corded—but at least two species of which are
known to be tied to Octocorallia (and one A.
gorgonophila showed ingested eggs with
adjacent tissue). Are those arthropods para-
sites of the corals, or are these Solenogastres
(especially P. sluiteri) genuinely omnivorous?

Some of the data given and repeatedly
cited in the literature is misleading. Probably
due to lack of interest, gut contents simply
were not noticed or not looked at accurately
enough. This is demonstrated in several rein-
vestigated species (See Table 2) and is strik-
ingly obvious in some neomeniomorphs:
Archaeomenia prisca sectioned and de-
scribed by Thiele (1906) as well as Neomenia
carinata (cf. Nierstrasz & Stork, 1940) contain
a large food mass in their gut lumen within
which the numerous spirocysts and nemato-
cysts are clearly discernible. On the other
hand, Nierstrasz (1902: 27) reports for
Hemimenia intermedia that “the animal feeds
оп sponge; in one of the specimens the ali-
mentary canal is filled with remains of food,
amongst which there are numerous sponge
spicules.” A reexamination of the slides re-
veals that there is indeed in one specimen an
accumulation of sponge spicules. These
skeletal elements, however, are totally iso-
lated from the alimentary food mass and not
embedded in it; they are found in a location
clearly above those of the animal's respective
section planes. The actual food mass within
the gut in both specimens of H. intermedia
distinctly contains a large amount of spiro-
cysts and nematocysts, some of which are in
ill-defined (semi-digested) condition.

Some special conditions in epizoic species
may still be discussed: Метаютета
banyulensis, Rhopalomenia aglaopheniae,
Anamenia gorgonophila, and Strophomenia
indica have been recorded so abundantly
upon respective Cnidaria (see Table 2 and
references therein) that there can be no doubt

SALVINI-PLAWEN

380

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MOLLUSCAN DIGESTIVE SYSTEMS

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384

MOLLUSCAN DIGESTIVE SYSTEMS 385

about the biological relation of the soleno-
gaster to the hypobiont. Careful investigation
of those solenogastres, however, resulted in
the almost total lack of identifiable food parti-
cles respective to the cnidarian; only some
sporadic nematocysts in one specimen of Я.
aglaopheniae and of S. indica confirm the
feeding relation, and the single record of
ingested eggs in A. gorgonophila may like-
wise point to the hypobiont's tissue. But why
don't further individuals and animals of other
species likewise possess nematocysts? A
closer look at the animals demonstrates that
the Solenogastres are generally associated
with or coiled around the stem of the cnidarian
colony; that portion of the body wall is, how-
ever, commonly protected by the theca
or by dense skeleton and hence mostly de-
void of nematocysts. Moreover, except for
Anamenia, the species are without radula and
presumably take their food up by macerating
the body wall and sucking the liquefied tissue
of the prey, the chyle of which would therefore
only rarely also contain nematocysts and
other distinct food particles. For Anamenia
also an active uptake of cnidarian parasites
might be considered (as indicated above). It
might therefore be deceptive to infer the diets
solely on the basis of epizoic information (see
Eleutheromenia sierra, Pruvotina sopita, and
others).

Feeding mechanisms and digestion:
There is little direct information for Soleno-
gastres about the uptake of food. The detec-
tion of food appears to be modulated by the
preoral sense organ with its chemoreceptive
papillae as well as its heavily acting ciliary
bands, and the mechanical contact may be
effected by sensitive hairs (circum-atrial
setae; cf. Pruvot, 1891; Salvini-Plawen, 1968,
1969b). Observations made by Baba (1940)
on Epimenia verrucosa and by Barnard on
Dorymenia paucidentata (cf. Salvini-Plawen,
1978) evidence the actual usage of the pro-
truded radula to get food, and inferences from
anatomical conditions (Salvini-Plawen, 1967a,
b, 1978) likewise suggest the protrusion of the
radula to the tip of the foregut. The action and
employment of the radula can often be con-
cluded on the basis of its morphological and/or
functional type, and in several cases even
analogized to conditions found in gastropods:
the monoserial-monostichous radula (Don-
dersia, etc.) to the Monostichoglossa (=
Saccoglossa), the pectinid and serrate mono-
serial radulae (Anamenia, many Amphimeni-
idae, etc.) to the Aeolidiacea, the polystichous

radula (Proneomenia, etc.) to the Taenio-
glossa, or the serrate-biserial radulae (Sim-
rothiella, etc.) to certain Stenoglossa. The
hooked distichous radulae of many soleno-
gastrid genera correspond to jaw formations in
Polychaeta or Rotatoria and may be regarded
as typical seizing forceps.

With the possible exception of the radula of
Dorymenia usarpi and some further species
which may also feed themselves by brushing
microorganisms, all other radula types may
serve to attack Cnidaria (Salvini-Plawen,
1967b): first, in most Solenogastres some
secretions of the foregut glands brought into
direct contact with the prey can prevent the
discharge of nematocysts due to hyper-
viscosity (Salvini-Plawen, 1972b). Only after
the cnidarian tissue has been immunized is
the prey attacked by the radula or by the
enzymatically macerating foregut secretions
(see below). The actual uptake of the
Cnidaria-food by means of the radula occurs
either when larger pieces from the prey are
ripped and cut off (cf. Heuscher, 1892; Baba,
1940; Salvini-Plawen, 1978), or when the
prey’s body wall is forced open and tissue is
sucked as also in the case of radula-less
representatives (Salvini-Plawen, 1967b,
1972b).

Nearly 50 species (more than 25%) from
different families show reduction of the radula.
In these animals as in further representatives,
the frequent elaboration of a proboscis and/or
a sucking pump points to the uptake of lique-
fied food (cf. Salvini-Plawen, 1967b). As
demonstrated in Drepanomenia vampyrella
(cf. Heath, 1911) and experimentally evi-
denced in Epimenia verrucosa (cf. Baba,
1940) the foregut glands produce secretions
which dissolve food into chyle. In raduia-less
species chyle is already formed when the tip
of the foregut touches and even enters the
body wall of the Cnidaria (any cuticular or
skeletal covering is thereby penetrated).
Finally, swallowing of the food takes place
either with help of the shovelling radula or by
suction, thus conveying the food to the midgut.
If present, ciliary movement supports this
process. The transport of the food within the
midgut itself is realized by the weak but dis-
tinct muscularis, as well as by the middorsal
ciliation. The epithelial lining generally con-
sists homogeneously of secretive and resorp-
tive club-shaped cells containing numerous
granula and larger bodies or droplets. Diges-
tion first takes place extracellularly by means
of the contents of the cell portions apocrinely

386

cast off into the gut lumen. Isolated small
particles of the chyle (partly including nema-
tocysts) are then phagocytised and digested
intracellularly. The remains of food (nemato-
cysts, spicules, cuticle, fragments of tests,
etc.) are conveyed dorsally to the posterior,
and are released via the rectum without the
formation of a peritrophic membrane (and
hence of true faecal pellets).

3. Placophora

The Placophora (or Polyplacophora) are in
general dorsoventrally compressed molluscs
3mm to 330mm long, and their mantle is
covered by a chitinous cuticle and aragonite
bodies, middorsally replaced by eight large,
generally four-layered plates; the mantle cav-
ity surrounds the flat, ventrally-innervated foot
(see Adenopoda) as well as the simple head
(head disc), and it produces 6-88 pluralized
pairs of ctenidia. The mantle epithelium pro-
duces sensory papillae and out of them the
specialized so-called aesthetes (cf. Fischer,
1978; Fischer et al., 1980). The alimentary
tract is provided with paired esophageal and
midgut glands, and the narrowed intestine is
variously looped; the uniform radula pos-
sesses 17 teeth per transverse row, and there
is a distinct subradular sense organ. The peri-
cardioducts are elaborated to function as ex-
cretory organs (emunctoria). The sexes are
(with few exceptions) separate, and fertiliza-
tion is external. The Placophora are marine,
generally living upon hard bottoms predomi-
nantly in the littoral zone, and most members
feed microherbivorously by scraping algae.
There are about 600 Recent species classi-
fied in three orders.

Digestive system: Most information on the
placophoran alimentary condition comes from
early investigation, essentially supplemented
by Fretter’s study (1937); surveys are sum-
marized by Hoffmann (1930), Owen (1966a,
b), and Hyman (1967).

In the centre of the head disc the mouth
leads to a short oral tube, limited towards the
actual buccal cavity by a distinct sphincter;
both sections are of a cuticularized epithelium
with interspersed mucocytes (buccal glands).
There is a pair of dorsobuccal foregut glands
(salivary glands) of simple to compound sac-
cular configuration, and the subradular sac
with its dorsally elaborated bipartite sense
organ consists of glandular epithelium, some-
times even terminally forming a seemingly

SALVINI-PLAWEN

paired gland proper (cf. Hoffmann, 1930;
Salvini-Plawen, 1972c). Beginning with the
dorsal foregut glands, the subsequent, ento-
dermal esophagus (cf. Hammarsten & Runn-
strom, 1925: 273) is of an epithelium without
cuticle bearing a longitudinal differentiation
into ciliated and mucous bands; above the
entrance of the radula into the pharynx, the
esophagus enlarges to differentiate anteriorly
a pair of glandular pouches and to lead poste-
riorly into the tubular esophagus proper as
well as into the paired esophageal glands.
The radula apparatus exhibits an extensive
supporting system including a transverse
muscle bar, paired bolsters (cartilages and air
sacs), and a great variety of muscle bundles
(cf. Plate, 1897; Graham, 1973). The radula
itself is produced in a very long, straight
sheath and rests upon the radular membrane
(ribbon). The uniform organ of 17 teeth per
transverse row shows the second lateral ones
elaborated as a robust, strongly sclerotized
hook. As demonstrated by the developmental
pattern (cf. Sirenko & Minichev, 1975), those
latter hamate teeth are the unique remnants
of the originally monoserial radula, whereas
the marginal teeth (3rd-8th laterals) as well as
the rhachis plus the first laterals arise only
later from one radula plate each of which is
subsequently fragmented (Fig. 6).

atl DANS
Fr ASS.

DA SS

Cay

FIG. 6. Placophora: morphogenesis of the radula
(from Sirenko & Minichev, 1975); the lateral plate at
each side in c and the central plate in d each is
fragmented to become six and three teeth respec-
tively.

MOLLUSCAN DIGESTIVE SYSTEMS 387

The extensive esophageal glands or sugar
glands extend ventrally and are built up of
carbohydrase-secreting cells as well as sup-
porting cells arranged in numerous villi (cf.
Fretter, 1937). The short, ciliated esophagus
exhibits longitudinal ridges and is limited
against the stomach by a sphincter. The
stomach demonstrates a fairly unusual con-
figuration from a comparative point of view. In
some conservative conditions it represents a
scarcely enlarged portion which may be ex-
ternally delimited merely by an anterior con-
striction (see esophageal sphincter) and by
the openings of the midgut glands. More de-
tailed information is available for the more
elaborated types of stomachs in the majority
of Placophora which are characterized by the
differentiation of a variously shaped enlarge-
ment, the ventral sac (cf. Fretter, 1937). The
stomach proper appears to be represented by
a scarcely extended section directly continu-
ous between the esophagus and the intestine
(see Fig. 7A) which corresponds to the above
stomach of the conservative type. Its wall is
characterized by a dorsal and ventral ciliated
band, delimiting the “dorsal channel” at the
right side (Fretter, 1937); the wall of the (ven-
tral-) left side is largely expanded to form a
voluminous, ventrally-bent sac. This latter
organ often has a cuticularized epithelium
(Fretter, 1937) or but a ciliated one (Green-
field, 1972) and is underlain by a distinct
muscle. The dorsal-left and left areas of the
wall of the stomach continues to become—
after separation of the ventral sac—together
with the now merely gutter-like “dorsal chan-
nel” the anterior intestine. This right-sided
“gutter”/“dorsal channel” in its turn posteri-

===

‚ne

—

orly receives the (in adults) asymmetrically ar-
ranged outlets of the midgut glands; in
Lepidopleuridae this entire section (“gutter”/
“dorsal channel” with orifices of the glands)
has become separated from the anteriormost
intestine to form the so-called ‘ductus
choledochus” (Plate, 1901: 442).

The paired midgut or digestive glands after
metamorphosis become arranged in succes-
sion, the right gland being directed dorso-
anteriorly and the left one spreading postero-
ventrally (cf. Hammarsten & Runnstrôm,
1925); each gland is structured into tubules,
the ductules of which join together to form one
outlet. Their epithelium consists of two types
of cells scantily provided with cilia. The slen-
der to club-shaped digestive cells are char-
acterized by small vacuoles, fatty and lipoid
droplets, as well as a large distal vacuole pro-
vided with an irregular granular mass; the lat-
ter is extruded and frequently present in all
parts of the midgut as well as the faecal pel-
lets (cf. Fretter, 1937). The second, less fre-
quent type consists of fairly pyramidal cells
filled with spherules of calcium deposits (lime
cells, excretory cells; cf. Owen, 1966b: 79).

The intestine is increasingly looped accord-
ing to different levels of differentiation (cf.
Plate, 1901: 444 f), and must be divided in two
successive sections. The anterior section is
continuous from the stomach and extends to
the intestinal valve at about one-third of the
total length of the intestine. It is characterized
by the two longitudinal ciliary bands arising in
the stomach, and actually begins behind the
orifices of the midgut glands where the “gut-
ter’ flattens out ventrally and a transverse
ciliated band splits off from the ventral one to

FIG. 7. Schematic diagrams of the main features of the gastric region to compare the basic configuration in
A, Placophora in general; B, Placophora-Lepidopleuridae; C, Scaphopoda; D, Bivalvia and Gastropoda; E,
Siphonopoda (cephalopods). Arrows indicate movements of contents (save for absorption); cae = caecum,
de = “dorsal channel” and “ductus choledochus,” gs = gastric shield, int = intestine, op = openings of the
midgut glands, ps = protostyle, ri = ridge (typhlosole), sa = sorting area, vs = ventral sac of stomach.

388 SALVINI-PLAWEN

ют the (now equally ventral-positioned)
dorsal ciliated band; it is surrounded by inner
circular and outer longitudinal muscle fibers.
The bipartite intestinal valve is marked by
ciliated epithelium underlain by an anterior as
well as posterior constrictor muscle, thus
functioning as site for the formation of the
faecal pellets. The following posterior intes-
tine underlain by weak musculature shows
ciliated and glandular cells secreting non-
mucous droplets to coat the faecal pellets;
they are thus possibly responsible for the
elaboration of the peritrophic membrane evi-
denced in at least some species (cf. Peters,
1968). The longitudinally-ridged epithelium of
the rectum shows uniform, densely ciliated
cells. The anus is surrounded by a distinct
sphincter muscle.

Diets: The majority of Placophora are graz-
ing microherbivores, scraping off incrusting
algae, other minute organisms and pieces of
larger weeds; hence also nonorganic materi-
al, such as sand grains or sponge spicules,
may accidentally be taken up with the food.

Some exceptions to the predominant form
of feeding are known; there is even carnivory.
This has been evidenced especially in the
Mopaliidae, within which Mopalia grazes on
sessile or sedentary organisms such as
sponges, Cnidaria, Bryozoa, or even poly-
chaetes and bivalves. Placiphorella in the
same family has specialized predation by
trapping and ingesting free-moving organ-
isms. The anterior mantle region is extended
and enlarged to form a flap with which the prey
is trapped when stimulating the flap. In addi-
tion, a tentacled mantle lobe in front of the
head disc functions as the posterior limitation
of the trap cavity; when prey is captured
(small crustaceans, polychaetes, etc.), the
mantle-lobe is raised and the flap curled in-
ward which brings the prey nearer to the
mouth region to be seized (cf. McLean, 1962).
Probably some other species have also at-
tained a special diet such as Hanleya hanleyi
(Lepidopleuridae), abyssal specimens of
which feed on sponges (cf. Plate, 1899: 74).

Feeding and Digestion: The only detailed
information comes from Fretter (1937: 151 f).
who gives a comparative account of the con-
dition in Lepidochitona cinerea (L.) and
Acanthochitona fascicularis (L.) or A. com-
munis (Risso). Before feeding starts, the sub-
radular organ of the animal firmly pressed to
the bottom is protruded through the mouth to
test the substratum for food; in case of a posi-
tive result, the sensory organ is withdrawn

and the radula is projected to become fully
exposed and pressed upon the substratum.
Since the teeth are directed backwards, the
rasping effect is on the return pull of the
radula, drawing the food particles into the
buccal cavity. That subsequent testing and
rasping action is repeated with every bite. The
rasped particles are pressed dorsally by the
retracting radula, mixed with the mucus of the
buccal glands and lubricated by the secretion
of the so-called salivary glands. Transferred
to the ciliated roof of the foregut, the food
string is conveyed along the esophagus by
ciliary currents and mixed up with the amyloly-
tic enzyme from the esophageal glands. En-
tering the stomach, the food string is directed
by the ciliary bands into the ventral sac, into
which likewise the proteolytic secretion of the
digestive glands is transported by the oppo-
site beat of the cilia on the posterior bands of
the stomach (via the “dorsal channel”; Fig.
1A). Thus the food string and the enzymes
are mixed and disintegrated in the ventral sac
by its muscular action; there is no rotation of a
food-mucus column.

The ventral sac and the anterior intestine is
the predominant site of digestion which is
purely extracellular (except for some phago-
cytosis by amoebocytes). Due to the lack of
cellulase, certain quantities of unbroken and
hence unattacked algal cells remain undi-
gested. The products dissolved by digestion
and undigested food-mucus material is forced
by muscular activity from the ventral sac into
the intestine, where it is rotated by ciliary ac-
tion and dragged backwards. Owing to the
musculature of the anteriormost intestine and
the intestinal valve, the mucus-food material
is squeezed in between both regions, so that
the dissolved products are separated and
pressed anteriorly (!) into the ducts of the mid-
gut glands; there absorption takes place by
the digestive cells. The intestinal valve itself
fragments the undigested material to faecal
pellets which in the posterior intestine are
more compacted and provided with a peri-
trophic membrane.

4. Galeroconcha-Tryblidiida
(Monoplacophora)

The Tryblidiida are shell-bearing Mollusca
1.5 mm to 37 mm long, the mantle with shell
of which covers the whole body; the mantle
cavity extends peripedally and houses 5-6
pairs of modified ctenidia; the ventrally-

MOLLUSCAN DIGESTIVE SYSTEMS 389

innervated foot (see Adenopoda) is flat and
there is a distinct head with tentacle forma-
tions. The excretory organs (emunctoria),
gonads, and heart-auricles are pluralized.
The alimentary tract is provided with exten-
sive, paired esophageal and midgut glands,
and the narrowed intestine is coiled; the
radula has 11 teeth per transverse row. The
sexes are separate, and fertilization is ex-
ternal. The Tryblidiida are marine, bottom-
dwelling deposit-feeders including 7-11 Ве-
cent species; they constitute the grade of a
mere order of the class Galeroconcha with
predominantly extinct members, also includ-
ing the order Bellerophontida (or Bellero-
morpha) accepted to be likewise untorted (cf.
Salvini-Plawen, 1980).

Digestive system: Available information
on the anatomy, including the digestive sys-
tem of the group is restricted to Neopilina
galatheae (cf. Lemche & Wingstrand, 1959)
supplemented by some notes on other repre-
sentatives. The mouth opening with its dorsal
and ventral lip is bordered by flapped tenta-
cles and leads into a cuticularized buccal
cavity, the dorsocaudal portion of which is dif-
ferentiated into a subradular pouch with a
naked, glandular epithelium and the distally
elaborated subradular sense organ. The ad-
jacent pharyngeal foregut produces a dorso-
frontal, cuticular plate or single jaw, a frontal
diverticulum with epithelial glands, as well as
the caudally-extending radula apparatus.

Resting upon a supporting apparatus simi-
lar to that of the Placophora by exhibiting a
strong transverse muscle bar and a pair of
rod-like cartilages, the radula itself inserts on
the ribbon which is proximally underlain with
the pharyngeal subradular membrane. Pro-
duced in a slightly coiled sheath, the radula
consists of 11 teeth in each transverse row
(cf. McLean, 1979). Except in N. (Vema)
hyalina, the three median teeth are fairly
slender, rod-like structures, while the second,
third, and fifth lateral teeth are broad hooks
with a blunt free end (as are also the first ones
in V. hyalina). The fourth lateral (or first mar-
ginal) teeth are more delicate structures hav-
ing a distal, aborally curved comb or brush of
about 30—45 slender, fringe-like denticles (for
details cf. McLean, 1979).

The transition from the pharyngeal foregut
to the ciliated esophagus is characterized by
a pair of lateral diverticula extending as flat
sacs beneath the dorsal body wall; they in-
clude three pair of pouches as well as the
so-called “dorsal coeloms” which, however,

in N. (Vema) ewingi are shown to be direct
continuations of those diverticula (Lemche &
Wingstrand, 1959: 56 footnote, and 1960:
1820). These extensive sacs are homo-
geneously lined with secretory epithelium,
and due to their identical configuration in
Placophora (cf. Fretter, 1937: fig. 1), they may
be homologized with the esophageal pouches
as well as esophageal or sugar glands in
these organisms (Lemche & Wingstrand,
1960: 1798 and 1820; Salvini-Plawen, 1972c:
279 f). The roughly triangular stomach re-
ceives the outlets of the extensively ramified,
paired digestive glands through a slit-like
opening at each side. The intestine, which is
overlain by a blind pocket, starts at the mid-
posterior. In the pocket a true crystalline style
seems to be produced, which possesses a
concentric structure and is directed towards
the esophageal opening; however, no forma-
tion of a gastric shield is said to exist. The
midgut or digestive glands are homogeneous-
ly lined with a high epithelium, the cells of
which contain several large peripheral gran-
ules and often also more basal, smaller gran-
ula. These cells would therefore correspond
to the secretive-absorptive, digestive cells of
other Conchifera (cf. Owen, 1966b: 80). The
long, ciliated intestine is coiled to form a flat-
tened cone (Lemche & Wingstrand, 1959;
Menzies & Layton, 1962: 406; Rokop, 1972;
Cesari & Guidastri, 1976: 235; McLean,
1979); in N. galatheae it consists of six loops
arranged counter-clockwise. The short, like-
wise ciliated rectum opens middorsally on a
low papilla into the posterior mantle cavity.
Diets: Information on the diets of Neopilina
comes only from analysis of gut contents. In
N. galatheae it included “a high proportion of
radiolarians, scattered centric diatoms, etc.
mixed up with much undefined detritus mat-
ter” (Lemche & Wingstrand, 1959: 63), and “a
faecal pellet removed from the hindgut of a
specimen of Neopilina (Vema) ewingi showed
the presence of diatom frustules, a radiolar-
ian skeleton, pelagic foraminiferal tests and
innumerable bacteria-size particles as well
as sponge spicules” (Menzies et al., 1959:
179); one V. hyalina also contained “diatom
frustules and sponge spicules in the gut”
(McLean, 1979: 13), and a South Atlantic
specimen contained the test of a foraminifer
shown by transmitted light (probably within
the esophageal gland; cf. Rosewater, 1970).
Filatova et al. (1974) briefly discuss the food
conditions of those representatives which ad-
here to hard substrates as recorded by

390

Filatova et al. (1968) in situ from the surface
of a large basalt rock, or also by Lowenstam
(1978) and McLean (1979). Accordingly, one
can accept that the diets in these animals
consist of the bacterial film and the layer of
organic debris “usually existing on the surface
of such hard substratum” (Filatova et al.,
1974: 675). All this evidence (cf. also Wolff,
1961) suggests that Neopilina in general is a
non-selective deposit feeder (cf. also Menzies
et al., 1959: 179/180). The probability of de-
posit-feeding is further supported by the dark-
coloured content within the intestine of N.
oligotropha and another Central-North Pacific
specimen (Filatova et al., 1968; Rokop,
1972).

Feeding mechanisms and digestion: No
observation is available on food uptake by
Neopilina. Owing to the analysis of the mus-
culature of the radula apparatus given by
Lemche & Wingstrand (1959: 39 f), there is
indication “that the radula carries the food
inwards by simply moving to and fro, without
being protruded through the mouth for real
rasping movements” (loc. cit.: 46). Hence, the
gathering of food is proposed to be realized
by the preoral tentacle apparatus (Lemche &
Wingstrand, 1959: 24; Wolff, 1961: 135;
Cesari & Guidastri, 1976: 238); the distance
of the head from the bottom in living animals
(cf. Lowenstam, 1978) supports that sugges-
tion. However, with respect to the proximity of
the radula to the mouth opening as well as to
the structure of the radula teeth, there may
well be an additional brushing and/or shovel-
ling function of the only slightly protruded and
displayed radula in gathering deposit material
(cf. also Filatova et al., 1974).

The food taken up is transported back-
wards to the esophageal foregut where it is
conveyed farther by the cilia. According to the
likewise ciliated stomach, this organ may
merely function to mix up the food particles
with enzymes of the crystalline style and to
sort out the faecal material. The real site of
digestion may therefore be the digestive di-
verticula, the peripheral end of the cells of
which often project like a tongue into the
lumen (Lemche & Wingstrand, 1959: 30) and
may thus indicate phagocytosis. Additionally,
the highly lobulated gland configuration also
points to intracellular digestion within these
organs; there are no allusions as to whether
extracellular digestion also takes place (cf.
also Owen, 1966b: 65 f).

With regard to the continuous faecal mass
within the intestine of Neopilina galatheae, N.

SALVINI-PLAWEN

oligotropha, and V. hyalina (Lemche & Wing-
strand, 1959; Rokop, 1972; McLean, 1979),
as well as to the photographed faecal ‘pellet’
of V. ewingi (Menzies et al., 1959: 179), there
seems to be no peritrophic membrane.

5. Other Conchifera

As mentioned, the alimentary conditions in
Gastropoda, Bivalvia, and Siphonopoda
(cephalopods) are in general more intensively
investigated and knowledge about them is
more broadly distributed, so that a summary
recalling the main features (as far as known)
will be sufficient.

Gastropoda: As concerns a comparative
analysis within the gastropods, especially the
conditions in Prosobranchia are of impor-
tance; essential studies on them come from
Graham (1939, 1949), Fretter & Graham
(1962), and Morton (1953, 1955); a most val-
uable summary is given by Owen (1966a, b).

The anterior alimentary tract is provided
with some scattered glands in the oral tube
(buccal glands), with a subradular sac to
which in Neritopsina (and several Neogastro-
рода?) ventral foregut glands are associated
(cf. Fretter & Graham, 1962: 156 and 165;
Starmühlner, 1959; Ponder, 1973), with later-
al buccal pouches, with diffuse (Zeugo-
branchs) or pairedly-distinct dorsal foregut
glands (salivary glands), and in most archaeo-
gastropods as well as mesogastropods with
glandular esophageal pouches; these esopha-
geal gland(s) in Neogastropoda are differen-
tiated to the unpaired gland of Leiblein and
poison gland (Toxoglossa) respectively (cf.
Ponder, 1973). There is a distinct dorsal jaw,
paired or single (cf. Fretter & Graham, 1962:
169), and some species possess a subradular
organ (cf. Hyman, 1967: 247). The primitive
radula of Gastropoda is rhipidoglossate;
morphogenetic data may suggest, however, a
distichous to biserial radula as original for
gastropods (cf. Kerth, 1979; also Sirenko &
Minichev, 1975), whereas the larval radula in
Patella is triserial with a three-cusped median
tooth (Smith, 1935) and in Onchidella the
median teeth precede the others (cf. also
Raven, 1958: 235).

The features of the stomach of the con-
servative members of the gastropods (see
archaeogastropods) are characterized by a
proximal globular region provided with a
coiled caecum, with the openings of the

MOLLUSCAN DIGESTIVE SYSTEMS 391

paired midgut glands, with a cuticularized
area (gastaric shield) against which the food-
mucus column (protostyle) is rotated and
mixed with enzymes, and with a ridged, cili-
ated sorting area; the distal tubular region or
style sac contains the major part of the proto-
style to become distally fractionated, and the
intestinal groove bounded by the two longi-
tudinal ridges or typhlosoles to convey non-
absorbed material to the intestine. More ad-
vanced microherbivorous Gastropoda (espe-
cially if provided with ciliary feeding mechan-
isms) have differentiated a true crystalline
style, a purely hyaline rod with a more liquid
core; the style sac then being functionally no
more continuous with the intestine but solely
by way of the intestinal groove. Digestion is in
part extracellular (stomach) and partly intra-
cellular (midgut glands; amoebocytes). Con-
stant herbivorous members show predomi-
nantly intracellular digestion, whereas in other
prosobranchs extracellular digestion appears
to predominate (cf. Owen, 1966b); investi-
gated Fissurellidae obviously perform solely
extracellular digestion (cf. Owen, 1958).

Macrofeeding, carnivorous or sucking
gastropods have generally abandoned the
style sac stomach (as have the algae-scraping
Patellida; cf. Fretter & Graham, 1962: 225 f)
and replaced it by mechanically acting organs
(muscular and cuticular equipments: giz-
zards), by histolytic secretions, or simply by a
thorough radular trituration of the food (see
Heteropoda, Ptenoglossa, Neogastropoda,
etc.). At least in some gastropods the exist-
ence of peritrophic membranes has been evi-
denced (cf. Peters, 1968).

Bivalvia: With respect to the evolutionary
differentiation found in Recent bivalves, four
main developmental levels correlated with
feeding conditions can be discerned: Ctenidio-
branchia (Nuculida), Palaeobranchia (Sole-
myida), Autobranchia (Lamellibranchia s. str.),
and Septibranchia (Poromyida; cf. Salvini-
Plawen 1980, 1981). As concerns the alimen-
tary tract and its special function, Owen (1955,
1956), Yonge (1928, 1939), Purchon (1956,
1957,1958), Reid (1965) and Judd (1979)
have contributed greatly to the present knowl-
edge which is surveyed in detail by Owen
(1966a, b).

Since the Bivalvia have lost the buccal
mass including the radula, jaw, subradular
organ, and pharyngeal glands, the most elab-
orated region of the gut is seen in the stom-
ach; rudimentary esophageal glands, how-
ever, have been reported to exist in Nuculidae

(cf. Pelseneer, 1891: 235-236; Salvini-
Plawen, 1972c: 279-280). The stomach ex-
hibits a similar elaboration of its complexity as
in gastropods (cf. summary by Nevesskaya
et al., 1971). The pyriform style sac organ of
protobranchs (Ctenidiobranchia and Paleo-
branchia) differentiates a food-mucus column
or protostyle with its functional and structural
attributes as in conservative Prosobranchia,
but there is no caecum (see Fig. 7D); in
Nuculidae digestion takes place extracellular-
ly (cf. Owen, 1956 and 1966b: 67). The great
majority of bivalves, the Autobranchia, on the
contrary have a true crystalline style with an at
least functional isolation of its distal portion
from the adjacent intestine. Among those two
principal types of elaboration, there is a cer-
tain variety according to the arrangement of
the single structures (as presented compara-
tively by Nevesskaya et al., 1971) which gen-
erally also correspond to systematic group-
ings.

In contrast to Yonge (1928) and Purchon
(1963), however, the similarities of the stom-
ach in Septibranchia to that in protobranchs
are—at least in Verticordiacea—due to sec-
ondary conditions. The investigations of Allen
& Turner (1974) and of Bernard (1974) con-
vincingly demonstrate that the Verticordiacea
belong to the autobranch Anomalodesmata.
On the other hand, the septum as well as the
similarly modified configuration of the stom-
ach in Verticordiacea and Septibranchia s. str.
(Poromyida) are clear analogies due to a
similar carnivorous diet (cf. Salvini-Plawen,
1980: 263).

Scaphopoda: п comparison to the major
conchiferan groups, there are only a few in-
vestigations of the alimentary condition in
Scaphopoda about which general information
can be discussed (cf. Morton, 1959; Sahl-
mann, 1973).

The head is scarcely elaborated (rather
than “reduced”), but there is an enlarged,
contractile but not retractile conical snout (oral
cone, but not “proboscis”) with the central
mouth and the two captacula-bearing bulges
at its base. The horizontally slit-like mouth
opening leads to a short buccal cavity pro-
vided with glandular lateral pouches. The
subsequent pharynx is characterized by a
strong, horseshoe-shaped jaw, by a small
subradular organ with ventrolaterally adjacent,
subepithelial gland cells, and by the strong
radula uniformly provided with five teeth per
transverse row. The esophagus with ciliated
cells and mucocytes demonstrates lobed en-

392

largements, the esophageal glands, and con-
tinues without distinct limitation in the fairly
thin-walled stomach. It is a muscular organ the
ventral and lateral epithelium of which is cuti-
cularized to be raised at one point to a small
tooth (gastric shield), but is devoid of muco-
cytes and ciliated cells (cf. Morton, 1959). The
midgut glands open proximally by means of
two large symmetrical orifices at each side of
a small ciliated caecum (Dentaliida) or but by
one single left opening (Siphonodentaliida). A
series of ciliated ridges radiates over the prox-
imal end of the stomach (sorting area). The
intestine without mucocytes performs a few
(generally three) loops and terminates in an
enlarged rectum to which a rectal gland is as-
sociated; it possibly serves for excretion of
lipid-containing metabolic products (Sahl-
mann, 1973).

The Scaphopoda feed on small organisms,
especially Foraminifera, but Dentalium entale
feeds also on Ostracoda and small molluscs
(Kelliella, Rissoa; Sahlmann, 1973). The food
is collected by the terminal, sensitive and
even adhesive bulb of the hydrostatically ex-
tended captacula (cf. Dinamani, 1964;
Gainey, 1972; Sahlmann, 1973). Larger prey
is grasped by the tip of the captaculum and
directly brought to the mouth by retraction of
the tentacle; smaller particles are conveyed
by ciliar tracts along the captaculum to the
mouth (not confirmed by Sahlmann, 1973), or
may also be taken up by the cone-like foot via
a dorsally formed groove. Ciliated labial
lappets pass the food material to the mouth
opening and from there by muscular action of
the oral cone into the buccal cavity. The food
is seized and thoroughly triturated by the
powerful radula (the counterpart of the jaw),
so that all organisms are fractured and only the
broken remains can subsequently be ob-
served. Peristaltic movements of the foregut
aided by the radula transfer the food mass to
the esophagus where it is provided with
glandular products and passed by ciliary ac-
tion to the stomach. There the material is pro-
vided with the secretion from the midgut
glands and mixed up by means of the muscu-
lar action of the stomach. Digestion is extra-
cellular and the contractions of the stomach
also press the dissolved products into the
digestive glands where they are resorbed.
Peristaltic movements finally squeeze the in-

SALVINI-PLAWEN

digestible remains periodically into the intes-
tine. The faeces are not compacted into sepa-
rate firm pellets, so that no peritrophic mem-
brane appears to be produced.

Siphonopoda (cephalopods)*: With re-
spect to the accurate synopsis by Bidder
(1966) and the clearance of the morpho-
genesis of the alimentary canal by more re-
cent studies (cf. Boletzky, 1967; Fuchs, 1973;
Meister & Fioroni, 1976), only some principal
conditions need be summarized.

Most living Siphonopoda are active macro-
phagous feeders, taking even carrion (Nauti-
lus), thus being predatory or scavengers.
Some lesser known members, such as the
Cirromorpha, collect small, planktonic food
and may be regarded as microvorous (cf. also
the loss of the radula). The prominent buccal
apparatus includes the characteristic jaws
(mandibles), the radula organ, and one
(Nautilus) or three to four sets of foregut
glands. The radula itself bears 13 teeth or
plates per transverse row in Nautilus, and
nine or seven elements in the Coleoida; dur-
ing radulogenesis in Loligo and Ozaena (=
Eledone) the median teeth precede the lateral
ones (cf. Fuchs, 1973). The ventrolateral
glandular lobes in Nautilus may correspond to
the paired anterior foregut glands of others
which open above the radula in the lower por-
tion of the dorsal buccal cavity; the posterior
foregut glands (poison glands) secrete to a
median duct which opens on a large papilla
below the subradular pouch, and the sub-
lingual as well as also dorsal buccal glands (if
present; cf. Fuchs, 1973) constitute median
masses of the ventral and dorsal portion re-
spectively of the central buccal mass. In
Nautilus a subradular organ is present.

The posterior esophagus, in Nautilus and
Octobrachia enlarged to form a crop, is of
entodermal origin as is all the subsequent
alimentary tract subdivided into stomach,
spirally coiled caecum with initially paired
midgut gland, intestine and ink sac. Except in
Nautilus, the fused midgut glands are sub-
divided into two portions referred to as diges-
tive gland (“liver”; distal section) and diges-
tive appendages (“рапсгеа$”; proximal sec-
tion) (cf. Bidder, 1976). There are two grooves
separated by a so-called columellar ridge
which convey from the midgut gland opening
through the caecum, Esophagus, crop, and

4Since the more recent re-establishment of earlier findings demonstrated that the arms are in fact cerebrally-innervated
organs and hence head-tentacles (rather than derivates of the foot), the erroneous term “Cephalopoda” should be sup-
pressed in favour of Siphonopoda Lankester, 1877 (cf. Salvini-Plawen, 1980a: 265, 1980b).

MOLLUSCAN DIGESTIVE SYSTEMS 393

stomach have a cuticular lining, the caecum
and the intestine are at least partially ciliated.
Movement of the food along the alimentary
canal is performed by muscular action (Bid-
der, 1966: 111). Digestion by enzymes com-
ing from the digestive gland(s) appears to be
completely extracellular and is carried out in
the gastric as well as caecal section. Absorp-
tion of digested food products occurs in the
digestive gland (“liver”) and caecum (Маий-
lus, Sepia, Octopus), but in Loligo only the
caecum (and part of the intestine) serves for
absorption.

B) EVOLUTIONARY PATHWAYS

Although there are still gaps in our knowl-
edge of the detailed alimentary conditions, the
configuration as well as principal function of
this organ system can be compared. In con-
trast to most previous considerations, the
present study also includes for the first time
equivalent data on the lower molluscs and
can thus more adequately enter into a dis-
cussion from the phylogenetic point of view.

1. Comparative analysis

In an earlier study (Salvini-Plawen, 1972c)
the organization of the molluscan groups has
already been compared with special refer-
ence to the Caudofoveata and Solenogastres
in the attempt to trace the homologous deriva-
tives of the different organ systems including
the alimentary tract. Greater knowledge now
permits me to give more precise information
and to contribute more essentially to the esti-
mation of conservative and advanced char-
acters.

Beginning with the radula, there is no doubt
about the principal homology of the organ
throughout the phylum. Except for the
Solenogastres (and Bivalves), all other
groups also demonstrate a radular membrane
or ribbon upon which the teeth are inserted
during radulogenesis; in Caudofoveata,
Placophora, Neopilina, Prosobranchia, and
Coleoida the ribbon is formed by the lower/
anterior odontoblasts, and the teeth them-
selves by the terminal ones (cf. also Raven,
1958: 233). The roof epithelium of the radula
sheath also contributes in general as con-
cerns special hardening processes. The con-
dition in Solenogastres—solely possessing a
basal cuticle continuous with the pharyngeal

cuticle, as is the elastic subradular membrane
in other molluscs (cf. Hyman, 1967: 236;
Scheltema, 1978: fig. 2)—at the first view may
either express a more conservative, or rather
a specialized state; the poorly elaborated
radula support in many species suggests a
primitive condition. On the other hand, it must
be pointed to the developmental pattern of
radulae in Solenogastres and Placophora
(compare Figs. 5 and 6) which exactly coin-
cide in their originally monoserial configura-
tion, independent of the later radiative spe-
cialization (esp. in Solenogastres, cf. Figs. 4
and 5). As is argued by Sirenko & Minichev
(1975: 432), the polyserial radula of the
Conchifera may morphogenetically be sub-
sequent to the actual (advanced) placophoran
condition—as appears indeed supported by
the radulogenesis in Pulmonata (cf. Kerth,
1979); the preceding formation of the central
teeth in Coleoida (Loligo, Ozaena) and
Gymnomorpha (Onchidella) may reflect an
advanced condition.

The formation of a single or divided jaw (or
mandible) despite its different elaboration
respective to the groups doubtlessly is
homologous throughout; it constitutes a prin-
cipal character of the level of Conchifera.

Immediately associated with the radula to
house its ventrally-bent section, a subradular
pouch or sac may be differentiated. This is not
only likewise the site for the subradular sense
organ in Placophora and more conservative
Conchifera, but is also correlated to glandular
organs. This can be stated in Placophora,
Neopilina, Gastropoda-Neritopsina, Scapho-
poda (rudimentary), and perhaps even in
Siphonopoda-Coleoida (posterior foregut
glands); the ventral foregut glands in Soleno-
gastres as well as the ventral glandular folli-
cles in Caudofoveata (opening with a papilla)
correspond exactly to such (at least distally)
paired glandular formations ventral to the
radula. Secondly, also the dorsal foregut
glands in Caudofoveata, Solenogastres,
Placophora, and Tryblidiida (frontal gland)
can be compared. With regard to the lack of
dorsal glands in Neritopsina and to their dif-
fuse arrangement in many other Archaeo-
gastropoda, however, doubts must be ex-
pressed about the homology of the gastropod
dorsal glands (salivary glands) with those of
the Aculifera; rather they constitute new dif-
ferentiation within the gastropod level.

There is some difficulty as concerns the
homology of the esophagus and its deriva-
tives. There is essential identity of the whole

394 SALVINI-PLAWEN

configuration of esophageal pouches and
glands in Neopilina (pouched “pharyngeal
diverticula” including the “dorsal coeloms”)
and in Placophora that there can be no seri-
ous doubt about their mutual correspond-
ence; in Placophora, however, the esophagus
clearly originates from the entoderm (Ham-
marsten & Runnstróm, 1925: 273, which in
this respect fully coincides also with Kowa-
levsky's figures, 1883). On the other hand,
these esophageal elaborations far-reachingly
coincide with the glandular esophageal
pouches (archaeogastropods, mesogastro-
pods) and the unpaired esophageal gland
(neogastropods) in Prosobranchia being,
however, of ectodermal origin (cf. Raven,
1958: 157 and 229/230); there is no informa-
tion about the derivation of the esophageal
pouches/glands in Scaphopoda. As pointed
out elsewhere (Salvini-Plawen & Splechtna,
1979), homology does not forcibly depend on
the germ layers (identical origin), since sub-
stitutions and shifts of materials may occur
without cancelling the original differentiation;
thus homology is not always defined by the
formative material, but rather due to identical
hereditary information. With this respect, we
may perhaps also homologize all the post-
pharyngeal/pre-gastric gut sections in
Siphonopoda (cephalopods) with the
esophagus (being configurated as such any-
way) and the entodermal crop as a modified
esophageal pouch (entodermal in Placo-
phora, ectodermal in Prosobranchia),

The gastric region including the stomach
and the midgut glands needs a more detailed
discussion: (a) The comparability of the gas-
tric area is especially high in Gastropoda and
Bivalvia (cf. Graham, 1949), since it coincid-
ingly includes a proximal globular region with
the gastric shield, the orifices of the midgut
glands, and the sorting area, as well as a
tubular region including two typhlosoles which
limit the intestinal groove, and the style sac
with the protostyle (Fig. 7D). There is no
agreement, however, whether the spiral
caecum in archaeogastropods (and vestigial
in scaphopods?) is a primitive feature (cf.
Graham, 1949); it might well be differentiated
in connection with the uptake/digestion of
more selected algal food. Further gastric
elaboration, most obvious by the differentia-
tion of a true crystalline style, must clearly be
seen as convergence in gastropods and bi-
valves. (b) Moreover, the characters in the
stomach of Scaphopoda (cf. Morton, 1959)
permit derivation of the conditions from an

Outlined organ common to Gastropoda and
Bivalvia (Figs. 7C and D), but which aban-
dons the protostyle again; the small gastric
diverticulum may with doubt correspond to the
spiral caecum in archaeogastropods, or
rather constitute a roughly analogous forma-
tion. (с) Reducing the complicated conditions
in Siphonopoda (cephalopods) to the most
simplified scheme for equivalent comparison,
there is fair probability that it likewise derived
from a style-sac stomach (Fig. 7E). The
caecum would then represent the distally
elongated and separated section of the intes-
tinal groove including the (major?) typhlosole
(columellar ridge; cf. Graham, 1949) as well
as the orifices of the midgut glands; on the
other hand, the cuticularized stomach would
be the section of the style sac including the
relic of the gastric shield. (d) In addition, the
Placophora demonstrate some allusions to a
similar principal configuration (cf. Graham,
1949) including the two ridges of the anterior-
most intestine with the “dorsal channel’/
“gutter” between as typhlosoles with intestin-
al groove, and with the cuticularized sac as
relic of the gastric shield area; to this interpre-
tation, however, we cannot agree. The basic
configuration of the placophoran stomach is
distinctly different (Fig. 7A), since the outlets
of the midgut glands open into the terminal
section of the stomach proper (“dorsal chan-
nel”/“gutter”); moreover, both the ridges
bordering the “dorsal channel”/“gutter” ар-
pear to be nothing but the separations for the
two one-way systems (Fig. 7A, arrows), viz.
the digested food material moving posteriorly
towards the intestine, and the digestive
enzymes from the midgut glands anteriorly to
the anterior stomach (and ventral sac) as well
as the dissolved products from the anterior
intestine forward to the gland orifices (cf. Fret-
ter, 1937). Also, there is no food-mucus
column rotating against a cuticularized area,
and the ventral sac does not correspond in its
position to a function as gastric shield (even
when cuticularized) relative to the style sac.
Thus, the ventral sac simply appears to repre-
sent an enlargement for storage and digestion
in more advanced Placophora, comparable to
the crop in many pulmonates and opistho-
branchs (cf. Owen, 1966b: 55). Such different
configuration when compared to Gastropoda/
Bivalvia is underlined by the more specialized
condition in Lepidopleuridae, where the
“dorsal channel” is in fact separated to form a
“ductus choledochus” (Fig. 7B). (e) As far as
knowledge of the gastric condition in Tryblidi-

MOLLUSCAN DIGESTIVE SYSTEMS 395

ida permits evaluation of comparative analy-
sis (cf. Lemche & Wingstrand, 1959), there is
an independently-formed style-sac stomach
in Neopilina, dissimilar to other molluscan
configuration. The dorsally separated true
crystalline style, the scarcely differentiated,
ciliated stomach with lateral openings of the
midgut glands, as well as the already stated
lack of cuticularization (gastric shield) are dif-
ferent characters to those in Placophora as
well as higher Conchifera. (f) Whereas all
groups discussed above (Conchifera and
Placophora) principally coincide in their basic
midgut organization by the synorganized dif-
ferentiation of a stomach, a pair of lateral mid-
gut glands, an intestine, and even also of
esophageal glands, the organization т
Caudofoveaa appears to be quite apart.
There is an extensive, unpaired sac which—
due to the condition in Psilodens and Meta-
chaetoderma—can be stated as a longitudin-
al (!) separation of a once homogeneous
organ; secondly, there is a developmental
series of midgut elaboration in recent levels of
organizations which functionally parallels the
evolutionary differentiation of a stomach with
a protostyle. (g) Finally, the midgut system of
Solenogastres stands totally isolated among
the molluscs and coincides at most with that
of Nemertini or several Turbellaria.

The straight intestine in Caudofoveata is
the minor section separated off from the once
homogeneously voluminous midgut and thus
represents an analogous formation to the
looped organ in Placophora and Conchifera,
these being homologous throughout and hav-
ing differentiated by a narrowing and elonga-
tion of the whole posterior midgut (adaptation
to microherbivory). There is no intestine in
Solenogastres. Faecal pellets surrounded by
a peritrophic membrane are known in Caudo-
foveata, Placophora, and Gastropoda; they
are definitely absent in Solenogastres and
very probably absent in Tryblidiida.

2. Adaptive conditions

The original differentiations of all those ali-
mentary configurations outlined are a reflec-
tion of feeding conditions. In consideration of
correlations between diets and organization
of the alimentary tract, there is clear mutual
dependence of the style-sac type of stomach
from microvory (cf. Yonge, 1930); moreover,
there is even distinct co-existence of micro-

vory with the elaboration of midgut glands.
These relations hold good for the Caudo-
foveata, the Placophora, the Tryblidiida, the
Gastropoda and the Bivalvia. Within the
Scaphopoda, the basic configuration of the
stomach—by heredity being without doubt
ancestrally similar to that of Gastropoda-
Bivalvia (see Fig. 7)—accordingly has altered
secondarily and abandoned the differentiation
of a (proto-)style; such a condition can be
principally confirmed likewise in Siphono-
poda. Consequently, we cannot attribute to
the Scaphopoda a factual “(omni-)micro-
vorous” diet rather than “(micro-)carnivorous”
feeding, a statement which fully coincides
with the findings by Sahlmann (1973) and
which might explain the total lack of the style
(cf. also Yonge, 1930). In Placophora, the
actual lack of a (proto-)style, however, can be
accepted as being a primary condition due to
their evolutionary status nascendi of respec-
tive adaptations; in addition, the special
algae-scraping diet of tidal forms obviously
does not adaptively imply the elaboration of a
(proto-)style (compare also Patellida, p. 391).

In consideration of the special condition in
Solenogastres, they are clearly predatory-
carnivorous animals. With respect to the like-
wise carnivorous Siphonopoda (cephalo-
pods), Prosobranchia-Heteropoda, -Neogast-
ropoda, etc., or even Bivalvia-Septibranchia,
that diet does not involve or cause an involu-
tion or loss of the midgut glands. Moreover,
the progressive adaptation of the midgut mi-
crovory in Caudofoveata distinctly points to an
originally homogeneous organ before the
longitudinal separation of an intestine and a
midgut sac occurred. We may thus positively
accept that the homogeneous, straight midgut
of Solenogastres, merely provided with lateral
expansions due to the serial arrangement of
the dorsoventral muscle bundles, corre-
sponds to an original configuration conserva-
tively retained because of carnivory. Such an
estimation parallels the primitive state of the
radula (basal cuticle, support) likewise to be
judged as conservative; it also coincides with
the presumed original digestion. It was
thought for a long time that primitive digestion
in Mollusca was intracellular (cf. Graham,
1955; Owen, 1966b: 65); several more con-
servative groups however, show predominant
or exclusive extracellular digestion (Caudo-
foveata, Placophora, Prosobranchia-
Fissurellidae, Bivalvia-Nuculidae). This led
to the acceptance of an originally intra-
plus extra-cellular digestion—as in Soleno-

396

gastres—with subsequent trends either lead-
ing to an increase of intracellular digestion
(phagocytosis) or to a predominance of ex-
tracellular digestion (cf. Owen, 1966b: 65 f).

In transferring these results into a phylo-
genetic scheme, the evolutionary differentia-
tion of the radula as such, as well as the basi-
cally gliding-creeping habits of the archimol-
luscan organization (cf. Salvini-Plawen,
1972c, 1980, 1981; Trueman, 1975, 1976) dis-
tinctly point to a primitively microvorous
manner of living of the ancestral molluscs (cf.
also Graham, 1955) which gathered their food
by means of an evertible brushing or scraping
pharyngeal cuticle (radula rudiment). On the
other hand, there is clear evidence that both
the recent microvorously-feeding lines, the
Caudofoveata and the Placophora-Conchi-
fera, adapted independently restricted midgut
sacs for respective secretion of digestive en-
zymes. In connection with their organization
this brings us to the qualified conclusion that
diet must be attributed a principal key char-
acter in the basic molluscan radiation (cf.
Salvini-Plawen, 1972c, 1980, 1981): (1)
some ancestral molluscs still provided with an
aculiferan mantle cover (chitinous cuticle,
aragonitic scales) adopted a burrowing mode
of life in an attempt to exploit sediments rich in
food without much change of their diets. Such
adaptation involved changes towards a worm-
like shape—with the differentiation of a hydro-
static muscular tube for burrowing, the reduc-
tion of the ventrally-innervated gliding surface
and mere differentiation of the cerebrally-
innervated section to become the pedal
shield, as well as further anatomical conse-
quences (cf. Salvini-Plawen, 1972c, 1980,
1981); they thus represent a separate evolu-
tionary branch of Scutopoda, viz. the infaunal-
microvorous Caudofoveata. Their recent or-
ganization can hence be attributed to a great
extent to the positive selection pressures
upon the preference for a new habitat with
better food exploitation. (2) Other populations
continued to live epibenthically and separated
a rudimentary head for better food uptake
(Adenopoda; cf. Salvini-Plawen, 1972с,
1980, 1981). The exploitation of microor-
ganisms in the littoral zone subsequently
included not only the formation of more pro-
tective shell plates (arranged serially to en-
able rolling-up), but also the selection of a
stomach with paired midgut gland and a slen-
der intestine, of esophageal glands, as well as
of a subradular organ. Such adaptive organi-
zation to micro(herbi)vorous feeding gave rise

SALVINI-PLAWEN

to the level of Placophora. (3) Early placo-
phoran organization presumably invaded
sublittoral bottoms to enlarge the range of
food, which released the animals from rolling-
up protectively and enabled formation of a
homogenous shell: Conchifera (cf. Salvini-
Plawen, 1972c: 263, 1981). Nonselective
deposit-feeding by means of the brushing
radula was supplemented by tentacle forma-
tions (characteristic for all Conchifera, cf.
Salvini-Plawen, 1980: 268, 1981) and the
differentiation of a jaw rudiment. Such feeding
might also have been one of the decisive
properties for the survival of the Tryblidiida.
The organizationally more successful early
gastropods and primitive bivalves also sup-
planted the ancient tryblidiids ecologically, the
latter having been forced to withdraw into bio-
topes where they could stand the competition.
Nonselective deposit-feeding as performed
by Neopilina in this respect appears to be a
favourable prerequisite, since it is that food-
source in most benthic biotopes—including
otherwise obviously oligotrophic areas (cf.
Rokop, 1972)—which is found in sufficient
abundance for the tryblidiids and other de-
posit- and filter-feeding organisms to live on
(cf. Menzies et al., 1959; Filatova et al., 1968,
1974). (4) Nonselective deposit-feeding also
performed in ancestral Gastropoda (radula;
cf. Owen, 1966a: 20) and in primitive Bivalvia
(labial flaps; cf. Salvini-Plawen, 1980a: 262,
1980b) favoured a presumably monophyletic
differentiation of a food-mucus column or
protostyle in Conchifera, subsequently adap-
tively elaborated along three different lines to
become a crystalline style (Tryblidiida, Gas-
tropoda and Bivalvia); there is no confirma-
tion, however, as concerns a possible (sec-
ondary) modification of other gastric charac-
ters in recent Neopilina. (5) Micro-carnivor-
ous, macrovorous, and other predatory diets
as assumed in Scaphopoda, Siphonopoda
(cephalopods), Bivalvia-Septibranchia, and
several advanced groups in Gastropoda
(Heteropoda, Neogastropoda, Gymnosoma-
ta, etc.) involved independent abandonment
of the congenital style-sac type of stomach to
become respectively modified within the given
frame of basic conchiferan midgut configura-
tion. (6) The food relations of Solenogastres
to Cnidaria in general indicate that the whole
group adapted in its origin to the cnidarian
food source, supported by the fact that other
diets are only recognizable within the higher
members (Cavibelonia). Originating in still
aculiferan Adenopoda (cf. Salvini-Plawen,

MOLLUSCAN DIGESTIVE SYSTEMS 397

1972c, 1980, 1981), that evolutionary line
presumably adapted at an early stage to
secondary hard bottoms rich in Cnidaria
(Cnidaria-‘meadows,’ coral reefs), thus de-
veloping a wriggling-winding locomotion as-
suming a laterally narrowed shape (with its
respective anatomical consequences; cf.
Salvini-Plawen, 1972c, 1980, 1981). Their
straight midgut devoid of a differentiation into
stomach, digestive glands, and intestine, as
well as their primitive character of a radular
basal cuticle and radula support (or also the
lack of a subradular organ) are therefore due
to the early evolutionary deviation from micro-
phagy (and respective adaptations) towards
Cnidaria-vory. Within the molluscs, the
Solenogastres have thus obviously retained
the most conservative general configuration
of the digestive system.

SUMMARY

A comparative analysis of the molluscan
alimentary condition reveals that 1. The
Caudofoveata are microvorous animals which
differentiated a longitudinal separation of the
more posterior midgut into a large single mid-
gut sac and a slender, straight intestine; they
perform extracellular digestion. 2. The midgut
in Caudofoveata demonstrates a gradual ad-
aptation to microfeeding conditions resulting
in the presence of a food-mucus column (pro-
tostyle) and a primitive gastric shield in ad-
vanced members (Chaetodermatidae). 3. The
Solenogastres are Cnidaria-vorous predators
with a straight, merely pouched midgut per-
forming intra- and extracellular digestion, and
they are devoid of a true radular membrane
(ribbon). 4. The Tryblidiida are nonselective
deposit feeders by means of a brushing radu-
la and assisting tentacle formations as well as
a distinct jaw formation. 5. The Scaphopoda
are (micro-)carnivorous animals rather than
being (omni-)microvorous. 6. The basic
elaboration of the midgut developed inde-
pendently twice, viz. in Caudofoveata (midgut
sac, intestine) and in Placophora-Conchifera
(esophageal glands, stomach, midgut glands,
intestine). 7. The gastric elaboration in
Placophora is a differentiation sui generis. 8.
The gastric configuration in Scaphopoda and
Siphonopoda (cephalopods) can be deduced
from the basically similar condition in Gastro-
poda and Bivalvia. 9. The general configura-
tion of the digestive system in Solenogastres
(see item 3 above) reflects the most con-

servative condition within the molluscs. 10.
The digestive system largely reflects basic
behavioural selection pressures (with sub-
sequent morphological adaptations) in evolu-
tionary pathways of molluscan radiation.

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MOLLUSCAN DIGESTIVE SYSTEMS 399

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ZUSAMMENFASSUNG

ZUR EVOLUTION DES ERNÄHRUNGSSYSTEMS DER MOLLUSKEN
Luitfried v. Salvini-Plawen

Eine vergleichende Darstellung von Darmtrakt, Nahrung und Verdauung bei Mollusken bringt
folgende Ergebnisse: 1. Die Caudofoveata ernähren sich mikrovor und weisen eine Längs-
Unterteilung des hinteren Mitteldarmes in einen langen, umfangreichen Mitteldarmsack und in
ein gerades Intestinum auf. Die Verdauung erfolgt extrazellulär. 2. Die Mitteldarm-Verhältnisse
innerhalb der Caudofoveata zeigen eine zunehmende Anpassung an die Mikrovorie, welche

MOLLUSCAN DIGESTIVE SYSTEMS

letztlich zur Ausbildung eines verfestigten Nahrungs-Schleimstranges (Protostyl) und eines
Magenschildes führt (Chaetodermatidae). 3. Die Solenogastres sind Cnidaria-vore Rauber mit
einem einheitlichen, nur mit serialen Lateralausbuchtungen versehenen Mitteldarm, worin intra-
wie extrazellulare Verdauung erfolgt. Als einzige Molluskengruppe weisen sie keine Radular-
Membran auf und ihre Radulapolster sind meist sehr einfach. 4. Die Tryblidiida ernahren sich
unselektiv von Bodensatz (Mikroorganismen und Detritus), welchen sie mit Hilfe der kehrenden
Radula und der Tentakelbildungen aufnehmen. 5. Auf Grund der Ernahrungs- und Mitteldarm-
Verhältnisse sind die Scaphopoden nicht als (omni-)mikrovor, sondern als (mikro-)carnivor zu
beurteilen. 6. Der Mitteldarm-Ausbau in Caudofoveata (Mitteldarmsack, Intestinum) und in
Placophora-Conchifera (Oesophagealdrüsen, Magen, Mitteldarmdrüsen, Intestinum) ist
voneinander unabhängig aus einem einheitlichen Organ ohne Abschnittbildungen erfolgt. 7. Der
Ausbau des Magens bei Placophora ist als gruppeneigen festzustellen. 8. Die Mitteldarm-
Verhältnisse der Scaphopoda wie der Siphonopoda (Cephalopoden) können von einer
Ausprägung abgeleitet werden, wie sie prinzipiell bei Gastropoden und Muscheln vorliegt (Fig.
7). 9. Die allgemeinen Verhältnisse des Darmtraktes der Solenogastres (Punkt 3) spiegeln die
ursprünglichste Ausprägung innerhalb der Mollusken wider, welche durch einen frühzeitigen
Ubergang zur räuberischen Lebensweise erhalten blieb. 10. Das Ernährungssystem der Mol-
lusken lässt weitgehend den Selektionsdruck auf grundsätzliche Verhaltensweisen (mit davon
abhängigen morphologischen Veränderungen) erkennen, welche wesentlich zur evolutiven Dif-
ferenzierung in Grossgruppen beigetragen haben.

NOTES ADDED IN PROOF

401

While the present paper was in press, two
studies of interest appeared, viz. “Structure
and functional morphology of radular system
in Chaetoderma” (in Russian) by D. Ivanov
(Zool. Zhurn., 1979, 58: 1302-1306) and
“Comparative morphology of the radulae and
alimentary tracts in the Aplacophora” by A.
Scheltema (Malacologia, 1981, 20: 361-383).
Ivanov's analysis based upon whole mount
sections of preserved material appears only
restrictively reliable and contrasts to the his-
tological investigations as concerns the
musculature and configuration of the radula
apparatus (see pp. 373 and 375, and K.
Deimel, 1981, Dissertation University Wien:
“Die Muskulatur des Radulaapparates bei
Caudofoveata”).

The study by Scheltema (1981) generally
coincides with and corroborates the condi-
tions presented here. There are, however,
some discrepancies and/or errors which
should be clarified: 1) There is a distinct dif-
ference between a radular membrane (rib-
bon) and the basal cuticle of Solenogastres:
the basal cuticle is a direct continuation of the
pharyngeal cuticle (as is the subradular
membrane of other molluscs possessing a
ribbon), and it is hence not independently
formed at the bottom or blind end of the radula
sheath. There are different grades of elabora-
tion of the basal cuticle (cf. H. Nierstrasz,
1905, in Zool. Jahrb. Anat., 21: 655-701, and
1909, in Ergebn. Fortschr. Zool., 1: 239-306)

which may even totally lack or but be elabo-
rated towards a ribbon-like structure as in
Epimenia verrucosa (cf. Nierstrasz, 1905:
684; 1909: 267).—2) Also Salvini-Plawen
(1972c, 1978) regards the possession of
tubular foregut glands (ventral organs type A)
as primitive for Solenogastres (error by
Scheltema, 1981: table 1); and in contrast to
the statement by Scheltema (1981: 362),
within the primitive Solenogastres (order
Pholidoskepia) the Dondersiidae are ге-
garded as belonging to the conservative level
(monoserial radula, foregut glands, mantle
scales, development) rather than the
Wireniidae (Salvini-Plawen, 1978, 1980).—3)
The argumentation by Scheltema (1981: 378)
as concerns the (non-)homology of the pedal
shield in Caudofoveata fails, since the homol-
ogy refers to the position, structure, synor-
ganization, and innervation of the pedal shield
relative to an overall ventral gliding sole (cf. S.
Hoffman, 1949, and the corrected version in
Salvini-Plawen, 1972c) with which the scat-
tered/diffuse mucous cells fully correspond
(sole glands; arranged to lateral clusters in
most Caudofoveata and Solenogastres re-
spectively; cf. Salvini-Plawen 1972c: 225 and
294f, 1978: 16). The cuticle of the pedal shield
(main argument by Scheltema, 1981) in any
case represents a secondary (!) character
and has nothing to do with the advanced
homology.

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MALACOLOGIA, 1981, 21(1-2): 403—418

EVOLUTION OF CALCAREOUS HARDPARTS IN PRIMITIVE MOLLUSCS!

Winfried Haas

Institut fur Palaontologie der Universitat Bonn,
Nussalee 8, D-5300 Bonn 1, Germany

ABSTRACT

Our considerations on the evolution of molluscan calcareous hardparts are primarily based on
the placophorans because of their systematic position between the Conchifera and the “Apla-
сорпога” (Solenogastres and Caudofoveata). Shell formation т the Placophora is significantly
more primitive than in the Conchifera. Calcium carbonate secretion takes place without the aid of
a true periostracum underneath a rather unstabile glycoproteinaceous cuticle. A differentiated
periostracal groove is not developed but is present in its primordial stage. The epithelium
secreting the shell plates does not show any relevant differences from the epithelium of the
perinotum. This can also be seen as a primitive evolutionary stage. Thus, the Conchifera must
be derived from the Placophora and not vice versa as is often supposed, especially by paleon-
tologists. In view of these considerations, the condition with eight isolated shell plates in the
Placophora must be seen as a phylogenetically original character. In our view, the conchiferan
shell must be interpreted as a fusion of the eight shell plates of the placophorans. The larval
valves of the chitons are formed in a markedly more primitive way than the concha of the
conchiferans with their highly differentiated shell gland. The formation of the calcareous spines
or scales of the placophoran girdle takes place in cell invaginations of the epithelial papillae. In
that way, a Crystallization chamber is provided, protecting the biomineralizate against external
influences. The spines or scales in the mantle of the Solenogastres and Caudofoveata are
formed in the same way. Their mantle epithelium with the calcareous hardparts is homologous
with the perinotum epithelium and its mineralizates of the placophorans. The hypothesis that the
shell plates of the Placophora can be derived from the anlagen of primitive spines in the original
molluscan mantle is discussed. The acquisition of the shell plates of the Placophora respec-
tively, the concha of the Conchifera is a new development in the phylogeny of the molluscs.

INTRODUCTION

The early phylogeny of molluscs can hardly
be recognized by means of their fossil record
because the subdivision of the phylum must
have already taken place in the Precambrian.
On the one hand, we know few fossils and on
the other it is supposed that most primitive
molluscs did not possess hardparts easily
recognized to be of molluscan origin. So we
are mainly restricted to speculations based on
Recent forms. In this paper, the somewhat
neglected aspects of the formation of cal-
careous hardparts by the mantle with respect
to evolution will be discussed.

OBSERVATIONS AND INTERPRETATIONS

We begin with the Placophora which hold a
key position as we examine the problem of
molluscan shell evolution. A normal chiton
has eight shell plates encircled by a girdle or

1Dedicated to Prof. H. K. Erben at his sixtieth birthday.

perinotum which bears, in most cases, cal-
careous spines or scales and which is cov-
ered by a glycoproteinaceous cuticle. The
structure of the placophoran shell plates (Fig.
1) has been described in detail by Haas
(1972, 1976). A shell plate consists of three
layers. There is a very thin and incompletely
polymerized organic cover, which is not a true
periostracum, and two calcareous layers, the
tegmentum and the hypostracum, which
consist of aragonite. The tegmentum is made
up of rods of spherulite sectors (Fig. 1C) run-
ning in its uppermost part parallel to the sur-
face. Further ventrally, the tegmentum is
formed by spherulitic sectors directed ven-
trolaterally. The tegmentum contains canals
for the esthetes. The hypostracum is con-
structed of crossed lamellae (Fig. 1D). Com-
pared with the crossed lamellar structures of
the Conchifera, this has some special fea-
tures: the bundles of the crystal fibres are
combined in such a way that their crystallo-
graphic c-axis coincides with the bisectrix of

(403)

404 HAAS

these crossing fibres. In the Conchifera, the
c-axes of neighbouring fibre bundles enclose
an angle of about 110°. Here the elements of
the third order (third order lamellae) are
mostly combined into sheet-like second order

Ver
I

Ya
Ц am

elements (second order lamellae) which are
never present in the Placophora. In modern
chitons (Neoloricata Bergenhayn) the articu-
lamentum (Fig. 1B) is developed as an inter-
calation within the hypostracum. It is built up

FIG. 1. Morphology of an intermediate shell plate of a chiton (after Haas, 1976). A, whole plate; B, block
diagram showing the shell layers (for location see A); C, block diagram of the tegmentum; D, crossed
lamellar structure of the hypostracum with crystallographic axes (a, b, c). a, articulamentum; c, crossed
lamellar structure of the hypostracum; ec, esthete canal; h, hypostracum; m, myostracum; mae, macres-
thete; mie, micresthete; pp, properiostracum; t, tegmentum.

EVOLUTION OF MOLLUSCAN CALCAREOUS HARDPARTS 405

of spherulitic bundles. It serves for a better
insertion of the shell plates in the perinotum.
The myostracum, a prismatic layer, present in
all chitons, is a modification of the hypostra-
cum for muscle attachment (Haas, 1972).

The perinotal spines or scales have a rather
complicated outer shape with differentiated
ornamentation in most living chitons. All are
constructed of a simple spherulitic sector of
aragonite, showing a primitive mineralogic
structure. The mantle and its epithelia secrete
two products: the shell plates and the cuticula
of the girdle with the spiculae or scales (Fig.
2)

There is only a very small degree of differ-
entiation between the epithelium forming the
shell plates and the perinotal epithelium. A
primitive kind of periostracal groove (Fig. 3)
shows, to a certain extent, differentiation of its
wall proximal to the shell plate. The distal wall,
in contrast, is covered by normal perinotal epi-
thelium. The cells of the proximal wall of the
periostracal groove may play a role in provid-
ing tanning agents for the inner parts of the
cuticle forming the properiostracum.

In this context, some remarks must be
made concerning the definition of a perios-
tracum. A true periostracum as it appears in

FIG. 2. Cross section through the middle part of Lepidochitona cinerea (L.), showing the situation of the shell
and mantle. a, articulamentum of the succeeding shell plate; af, accessory fold of the perinotum; ct, ctenid-
ium; си, Cuticle; e, esthetes and esthete canals; f, foot; go, gonad; i, intestine; mg, midgut gland; pe,
perinotum epithelium; pn, perinotum; ppg, properiostracal groove; s, shell plate; se, epithelium secreting the
shell plates; sp, calcareous spine.

406 HAAS

the Conchifera is a pellicle covering the cal-
careous part of the shell consisting of poly-
merized organic material (tanned proteins),
which is formed in a periostracal groove en-
circling the shell border. The shell plates of
the Placophora are covered by a rather in-
significant organic pellicle, but it seems to be
only weakly polymerized. Its existence is
rather difficult to prove. This can be done if
one briefly decalcifies a shell plate. Then a
pellicle on which the distribution of the esthete
caps adhering to it show their original distri-
bution pattern (Haas, 1972) can be stripped
off. From morphological observations, it ap-
pears that a stabilization, perhaps by tanning,
of the proteinaceous content of the inner part
of the cuticle takes place on the shell plate at
some distance from the mantle edge. Be-
cause of technical difficulties, we have failed
to demonstrate the presence of tanning
agents by means of the DOPA-reaction.
Beedham & Trueman (1968) obtained a posi-
tive Millon reaction for proteins at the site of
the properiostracum. From its morphological

nature and because the properiostracal
groove in Placophora never contains any
polymerized pellicle, the organic cover of the
shell plates can only be seen as a first evolu-
tionary stage of a periostracum. Accordingly,
it should be called the “properiostracum.” In
contrast to the true periostracum in Conch-
ifera, it does not play an important role in shell
formation but may merely provide a protection
of the shell plates against corrosion.

The mode of calcium carbonate precipita-
tion in the tegmentum of the Placophora is
rather primitive. The cells of the mantle edge
surrounding the valves are covered with long
whip-like processes (microvilli) adjacent to the
shell margin (Fig. 4). Also, the cuticle from the
periostracal groove, which may be tanned to a
certain degree, covers the margin of the
valves. Thus, a crystallization chamber (Haas
& Kriesten, 1974; Haas, 1976) is provided
which, on the one hand, prevents any influ-
ence from the external environment and, on
the other hand, prevents calcium carbonate
secretion into the cuticular material covering

FIG. 3. Cross section through the shell and mantle near the shell margin in Acanthopleura granulata
(Gmelin), cu, cuticle; dw, distal wall of the properiostracal groove; pa, epithelial papilla of the perinotum; pn,
perinotum; pp, properiostracum; ppg, properiostracal groove; pw, proximal wall of the properiostracal

groove; sp, calcareous spine; t, tegmentum.

EVOLUTION OF MOLLUSCAN CALCAREOUS HARDPARTS 407

N
И SS A

> A

FIG. 4. Cross section through the shell and mantle near the shell margin in Lepidochitona cinerea (L.).
Cuticle and cell processes of the mantle edge protect the growing shell margin. cp, cell processes; cu,
cuticle; pp, properiostracum; ppg, properiostracal groove; t, tegmentum.

the valve margin. Although we cannot ob-
serve a true periostracal groove with the high
degree of differentiation of the Conchifera
(Fig. 5), nor a true periostracum, nor the high
degree of differentiation of the shell-secreting
conchiferan epithelium, we must state that the
Placophora possess around each shell plate
a primitive periostracal groove. The latter has
been called by Haas 4 Kriesten (1974) the
properiostracal groove. In Placophora, the
region between the proximal wall of the pro-
periostracum groove (Figs. 4, 5) and the shell
edge can be homologized with the outer man-
tle fold of the Conchifera (Haas, 1972). Then,
following this line of thinking, the perinotum is
homologous with the inner mantle folds of the
Conchifera (Haas, 1972).

As already noted, the shape of the perinotal
calcareous hardparts may be rather compli-
cated, although the structure itself is a simple
spherulitic sector of aragonite. The calcare-
ous part of a spine or scale can be secreted
by a single cell (Haas 4 Kriesten, 1975; Haas,
1976) or by an epithelial layer within an
epithelian papilla (Haas 8 Kriesten, 1977).
But also in the latter case, spine formation
begins with a one-cell stage. Fig. 6 shows the
formation of the calcareous part of a spine by
a single cell. At the beginning (Fig. 6A), this
cell is deeply invaginated and the calcium
carbonate is precipitated extracellularly in the
chamber thus formed. Later (Fig. 6B), the
growing spine protrudes from the epithelial
papilla and the neighbouring cells are in close

408 HAAS

TT
©

т Als IN AR
LE A
SS

oy | oa ое
ооо РВВ

ZO
FIG. 5. Situation of shell and mantle in the gastro-
pod Helisoma duryi (Wetherby) (after Chan 4
Saleuddin, 1974). if, interior mantle fold; meg, man-
tle edge gland; of, outer mantle fold; p, periostra-
cum, pc, periostracal cells; pg, periostracal groove;
s, shell.

10 um

contact with it forming a collar around the
shaft of the spine. They secrete an organic
pellicle onto the spine. Thus, a crystallization
chamber is provided. At the final stage of
spine formation, the neighbouring cells and
the cell which secretes the calcium carbonate
form the organic cup at the proximal end of
the spine. This cup is identical to the cup of
the macresthetes (Haas & Kriesten, 1975,
1977, 1978). Recently, Fischer, Maile &
Renner (1980) proved conclusively that
nearly all the elements of the esthete appara-
tus can be shown in certain epithelial papillae
of the perinotum. These observations support
strongly our assumption that differentiation of
the perinotal epithelium and the epithelium
secreting the shell plates, especially the teg-
umentum, is minimal.

Fig. 7 shows the epithelium forming a large
calcareous spine (megaspine) in Acantho-
pleura granulata. The formation begins with

INS
Y

Q \

Y N
E NN Е
4 N

IIA

FIG. 6. Schematic diagrams of two different stages of spine formation in Lepidochitona cinerea (L.). The
calcareous part of the spine is formed by a single cell. A, early stage; B, advanced stage. b, basal, calcium
carbonate-secreting cell; с, calcareous part of the spine; п, neighbouring cell; о, vesicles filled with organic
material which form the organic pellicle of the spine; p, organic pellicle of the spine.

EVOLUTION OF MOLLUSCAN CALCAREOUS HARDPARTS

My,
4,
y, 4%

77
4 iy Mi

CO |

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Uy ZINN

2 N
ААА
NS №

MTL LA A IN
А ee

(A АКА MS WS

“al М ® m №
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4 My
Ay, “ind |.
lp №
о ААА ww $
@ И | WN
, %, % vali ML a а К
ть ой aay Tes МА a ve
AN А Ss
О м Nh wa ede, м SAN
3 | “
4 Ny Mu ui null ni “a № ‘ N
’ OM yyy | (a a
NON 7, A wwii ull N У
A 4 \
м ии у rio ur
Чу, Чи, N"
Y у ae "a
AY “ay dA we
yyy i |

FIG. 7. Advanced stage in spine formation in Acanthopleura granulata (Gmelin). The calcareous part of the
spine is formed by many calcium carbonate-secreting cells, Symbols as in Fig. 6; pa, epithelial papilla of the

perinotum.

an invagination in a single cell as in the case
described above. Later this initial cell divides
and an epithelium secreting calcium carbon-
ate is formed. Some spines in living chitons
attain rather large size and continue to grow
throughout the animal's life (Plate, 1901). The
neighbouring cells play the same role in clos-
ing the crystallization chamber and producing
an organic рейсе as in spine formation by a
single cell. In the same way, an organic cup
may be formed as described above. The initial
papilla concerned with the spine formation
degenerates and other cells divide and pro-
duce new perinotal epithelium. As a whole,
the spine-secreting epithelium of the multi-
cellular type resembles very much the epithe-
lium secreting the tegmentum of the shell
plates. Obviously, one can compare to a cer-
tain extent spine formation with shell forma-
tion and can, in principle, attribute to each
spine its own periostracal groove as Kniprath
(1979) suggests. But, in our view this is not
reasonable because one can properly speak
of a periostracal groove only if it derived from
the true periostracal groove of the Conchifera.

There is an even more primitive mode of
calcareous spine formation observed т
young bottom-living larvae (Fig. 8) which may
also occur in the adults of certain primitive
chitons like Hanleya (Plate, 1901; modern ob-
servations are lacking). Here the calcareous
spine is formed within a deep invagination of a
papillar cell. In that case the apical part of the
cells forms a collar which closes the crystalli-
zation chamber at the basal part of the inva-
gination. There is no evidence that an organic
pellicle is formed. The neighbouring cells do
not seem to be involved in spine formation.

Shell formation in chiton larvae is also very
instructive with respect to our assumption that
shell formation in the Placophora is more
primitive than in the Conchifera (Haas, Kries-
ten & Watabe, 1979, 1980; Kniprath, 1979).
Here too, a crystallization chamber is pro-
vided to keep the biomineralizate free from
external influences and to guarantee proper
localization of calcium carbonate precipita-
tion. In young free-swimming larvae, the dor-
sal epithelium is differentiated into bulges and
grooves. At the site of the grooves, formation

410 HAAS

of the shell plates occurs later (Figs. 9, 10). As
we interpret this situation, the neighbouring
cells of the groove complex produce a type of
mucous cuticle which is rather unstabile and
which covers the site of later calcium carbon-
ate precipitation, closing it against external in-
fluences. The dorsal covering of the mantle in

CS
\ N) em
о Тит
x |
NUN
Ss = 7 |
fe a RA
SA AT SENS
Al eal
SS
Sr, va LÉ
ay A Ae
N, N
IN de
NU
Alo NS А
A NAS SP LIN
= SS <=
NA UNA Qs
ee м
ly) UNG Te
US
:b

FIG. 8. Spine formed by a single cell in the peri-
notum of larval Lepidochitona cinerea (L.). b, ba-
sal, calcium carbonate-secreting cell; sp, spine.

chiton larvae consists of a mucous layer of
rather low electron density which we consider
to be identical with the cuticle. At the apices of
some cells within the region between the
groove complexes, electron dense piliow-like
masses of organic material can be observed.
They seem to dissolve in the cuticle. This
phenomenon has been described by Ham-
marsten & Runnstrôm (1925) and by Kniprath
(1979). We have the impression that this con-
densed organic material is transported on the
grooves where later calcium carbonate pre-
cipitation takes place to achieve a better seal-
ing of the future crystallization chamber. The
organic material cannot be compared with the
Organic material forming the spine pellicle
which is secreted from small vesicles (see
Haas & Kriesten, 1975). We do not accept
Kniprath’s (1979) opinion that only the elec-
tron dense material represents the cuticle. It
has not yet been observed in the formation of
the perinotal cuticle. On the other hand, it
does appear in some sections through the
adult animals near the mantle edge where it
seems to be involved in the formation of the
organic cover of the shell plates. On the other
hand, we must admit that the dorsal covering
of chiton larvae is rather incompletely con-
sistent. But, while the first calcium carbonate
secretion appears, the entire valves are cov-
ered with a fibrous cuticle. However, little is
known about the formation of the placophoran
cuticle.

FIG. 9. Median section through the mantle of a free-swimming larva of Lepidochitona cinera (L.), showing
two groove complexes (after Haas, Kriesten & Watabe, 1980). cu, cuticle; gc, groove cell; gl, gland cell; gr,
groove; li, lipid granulum.

EVOLUTION OF MOLLUSCAN CALCAREOUS HARDPARTS 411

Later the groove complex proliferates, and
long cell processes (microvilli) interdigitate
from the edges of the crystallization chamber
forming a cage and keeping the biominerali-
zate in place (Fig. 11). The larval shell shows
spherulitic growth of aragonite. Later, a sim-
ple crossed lamellar layer is secreted and the
first two esthetes appear in the shell.

Compared with the highly complicated and
well programmed shell field development in
the Conchifera (Kniprath, 1977, 1979), the
development of the shell field in the Placo-
phora is primitive. In the conchiferan larvae, a
pellicle is formed at the distal edge of the in-
vaginated shell gland which must be desig-
nated а periostracum. In this way, a crystalli-
zation chamber is provided which is obviously

more perfect than the cuticle and microvilli
cage method in placophorans. A true perios-
tracum in larvae as well as in adults has the
main advantage for shell formation because
the first respectively lateral mineralizates of
the shell no longer need to be separated
against a cuticle. Consequently, the microvilli
cage can be given up. The outer shell layer
can now be directly precipitated against the
periostracum which provides a perfect closing
of the mineralization chamber against exterior
influences.

For our considerations the shape of the pe-
riostracal groove itself is not so relevant as is
its differentiated proximal wall. From this point
of view, homologization of the periostracal
grooves of Placophora and Conchifera is

lum

FIG. 10. Groove cell complex of a free-swimming larva of Lepidochitona cinerea (L.); detail of Fig. 9. be,
bulge cell; cp, cell processes; gc, groove cell; gr, groove.

412 HAAS

5 ит

FIG. 11. Median section through а bottom-dwelling larva of Lepidochitona cinerea (L.), showing calcium
carbonate secretion in an intermediate shell plate (after Haas, Kriesten & Watabe, 1980). cp, cell processes;

cu, Cuticle; li, lipid granule; s, shell plate.

possible. For this question it is more signifi-
cant that the proximal wall of the periostracal
groove, or the properiostracal groove and the
epithelium secreting the shell, form a mantle
fold enabling lateral growth of the shell. This
occurs both in the Placophora and the Conch-
ifera. Due to their manner of secreting their
outer shell layers, the inclination of the proxi-
mal wall of the outer mantle fold is funda-
mentally different in both groups. In the Pla-
cophora it is directed mesioventrally, whereas
in the Conchifera it is mostly horizontally dis-
played.

We have presented some observations and
speculations which suggest that shell forma-
tion in Placophora is more primitive than in
Conchifera. Next we must seek animals
which, with respect to their calcareous hard-
parts, are more primitive than the Placophora.
These are represented in the living Soleno-
gastres and Caudofoveata, comprised in the

stage group Aplacophora. In the living fauna,
these animals are highly adapted to special
life conditions (ciliary gliding and sediment
boring, respectively). According to Hoffman
(1949) and Boettger (1955), both are ho-
mologous in several respects with the Placo-
phora. The mantle of the Solenogastres and
Caudofoveata is covered with a cuticle con-
taining calcareous scales or spicules. Both
groups show in their papillate mantle epithe-
lium and in their calcareous hardparts con-
siderable similarities to the perinotal epithe-
lium of the Placophora. The spicules and
scales also consist of aragonitic spherulite
sectors which are in some cases covered with
an organic pellicle. In some Solenogastres,
the spicules bear an organic cup at their prox-
imal end (Hoffman, 1949). Some of the spi-
culae in more highly evolved Solenogastres
are hollow, whereas primitive forms possess
massive scales, spines or needles. The for-

EVOLUTION ОЕ MOLLUSCAN CALCAREOUS HARDPARTS 413

FIG. 12. Longitudinal section through the mantle of
a primitive solenogastre (gen. et sp. nov), with de-
veloping calcareous scales. b, basal, calcium car-
bonate-secreting cell; n, neighbouring cell; sc, cal-
careous scale.

mation of the calcareous hardparts in both
classes, despite some differences in the
morphology of the mantle epithelium, takes
place in nearly the same way (Figs. 12, 13) as
has been described above in the perinotal
hardparts of the Placophora, especially in the
spines of larvae or of very young metamor-
phosed animals (Fig. 8). It is out of the ques-
tion that the aplacophoran classes Soleno-
gastres and Caudofoveata are phylogeneti-
cally closely related to the placophorans.
Considering hardpart formation, such a rela-
tionship is not possible.

DISCUSSION

Many of the problems we have discussed in
the previous section must be viewed in the
context of the molluscan phylogenetic tree.
Fig. 14 is based on the author’s arguments on
the evolution of molluscan calcareous hard-

parts; it incorporates some features of the soft
body. In nearly all respects, this phylogenetic
tree conforms with the representation of mol-
luscan evolution conceived by Salvini-Plawen
(1972, 1980). For our purposes, we have in-
troduced combinations of taxonomic names
with the prefixes Archi- and Eu-, thus indicat-
ing that there are hypothetical stem groups
and existing groups. These names are of no
taxonomic significance.

It has long been debated whether the
Placophora descended from the Tryblidiida,
which are without any doubt Conchifera, by
subdivision of the concha into eight. shell
plates, or whether the Conchifera stem from
the Placophora by unification of their eight
shell plates into one concha. The former view
has been advocated recently mainly by pale-
ontologists (Knight, 1952; Runnegar & Pojeta,
1974). It is more reasonable to think that
Placophora are the ancestors of Conchifera.
For it is obvious—a point having been
stressed by Boettger (1955) and Salvini-
Plawen (1972)—that the dorsoventral mus-
cles of the chitons are arranged serially into
2 x 8 pairs and that in the Tryblidiida there

FIG. 13. Longitudinal section through the mantle of
Falcidens gutturosus (Kowalevsky) with a develop-
ing calcareous scale. b, basal, calcium carbonate-
secreting cell; cu, cuticle; mu, muscle bundle; n,
neighbouring cell; pa, epithelial papilla; sc, cal-
careous scale.

414 HAAS

Meee

Euconchifera Tryblidiida

Sarat

O Archiconchifera

= Euplacophora

= LF sg Ny

x
A ;

> ae

ot ae ©

Caudofoveata

Archiadenopoda

>
O
e
=
—
m
À
>

Archimollusca 7 S

Premolluscan Ancestors

FIG. 14. Phylogeny of the primitive Mollusca based on the evolution of the calcareous hard parts of the
mantle. Features of the soft body are taken from other authors, mainly from Salvini-Plawen (1972, 1980). |
did not follow the arguments of Boettger (1955) and Salvini-Plawen (1972, 1980) according to which all
primitive molluscs had only one pair of ctenidia.

EVOLUTION OF MOLLUSCAN CALCAREOUS HARDPARTS 415

are, in spite of the uniform concha, eight pairs.
In this latter case, the double cords of the
Placophora have been concentrated into sin-
gle cords. It is difficult to imagine why a uni-
form concha should have, preadaptively refer-
ring to polyplacophory, multiplied its dorso-
ventral muscles as in the case of the Try-
blidiida. The evolution from the Tryblidiida into
the different euconchiferan classes shows an
obvious reduction or concentration of the dor-
soventral muscles. This is by far the best
technical solution for animals which elevate
their shell above the substrate [as also Neo-
pilina does (Lowenstam, 1978)] and which
can withdraw their body into the shell. In this
context, the capacity for rolling up in the
Placophora would not be understandable in
an evolutionary way of a subdivision of the
concha. It is more convincing that the loss of
the placophoran longitudinal muscles ap-
peared during the evolution from the Placo-
phora in the direction of the Conchifera rather
than vice versa. This means that the rolling up
ability and the possession of longitudinal
muscles must be inherited from the ancestors
of the Placophora (Archiadenopoda). These
considerations, often presented by other
authors (see Salvini-Plawen, 1972, 1980), are
supported by shell formation in larvae as well
as in adults, and the low degree of differentia-
tion of the mantle epithelium in the Placo-
phora is obviously more primitive than in the
Conchifera.

An important problem in the hypothesized
derivation of the Conchifera from the Placo-
phora is the possession of crossed lamellar
structure in the chitons and, on the other
hand, the possession of the nacreous struc-
ture in the Tryblidiida. The nacreous structure
has been thought by various authors to be the
most primitive structure of the inner layer of
molluscan shells. This shell type is present in
the Tryblidiida and in all basal stocks of the
euconchiferan classes. In most of the latter,
the nacreous structure is abandoned in more
advanced phylogenetic stages in favour of a
crossed lamellar structure. Without referring
to some adventurous speculations arising
from lumping together the placophoran and
conchiferan crossed lamellar structures, we
come to the following conclusions. As we
have demonstrated earlier (Haas, 1972,
1976) and discussed in this paper, the
crossed lamellar structure of the placo-
phorans is in its mineralogical properties de-
cidedly different from the crossed lamellar
structure of the Placophora as a unique

apomorphic acquisition which has nothing to
do with similar structures in the Conchifera. It
is best to imagine that the Archiplacophora
have had a rather undifferentiated inner shell
layer which probably was made up of spheru-
litic sectors. From such a structure there have
evolved on the one hand the crossed lamellar
layer of the Placophora and the nacreous
layer of the Conchifera on the other.

Starting from our conclusion that the epithe-
lium secreting the shell plates and the epithe-
lium of the perinotum are not very different,
we may suppose that one can postulate a
genetic relation between the calcareous
hardparts of the placophoran mantle.

As mentioned above, several authors
(Blumrich, 1891; Runnegar, Pojeta, Taylor &
Collins, 1979) have proposed that the placo-
phoran shell plates must have been derived in
some way from megaspines. But megaspines
are only present in highly evolved chiton taxa
so that they must be supposed to be phylo-
genetically younger than shell plates. The
close similarity of the epithelia secreting both
shell plates and megaspines is therefore an
expression of the fact that the differentiation
of the respective mantle epithelia is rather
limited. It would also be difficult to understand
how the esthetes, which are specialized peri-
notal papillae, could be incorporated into a
megaspine.

It can be more easily imagined that the shell
plates of the Placophora have developed from
the anlagen of simple spines or scales as we
have described in the case of the perinotum of
larvae and young metamorphosed animals in
chitons or from the mantle of the Aplaco-
phora. However, derivation of the placo-
phoran shell plates from definite spines or
scales, especially from the highly specialized
calcareous perinotal hardparts in most chi-
tons, cannot be admitted. The evidence
against this view is their formation in a cell
invagination and the sealing of the crystalliza-
tion chamber by the collar mechanism pro-
vided by the cell apices or the neighbouring
cells. We must rather suppose that within
eight median areas of the mantle of those
Placophora (which we prefer to call Archi-
placophora), the calcium carbonate-secreting
cells do not invaginate as deeply as in normal
spine or scale formation. Consequently, a col-
lar mechanism which serves the shaping of a
single spine did not operate. Thus, calcium
carbonate precipitation could take place un-
derneath the cuticle from several calcium car-
bonate-secreting sites, forming a plate-like

416

biomineralizate. The deposited mineral could
incorporate sensitive papillae (now trans-
formed into esthetes). To give a definite
shape to such a primordial shell plate, a man-
tle edge, in order to enable lateral growth and
formation of new esthetes, and a seam of cell
processes, in order to prevent irregular crystal
growth into the cuticle, have become neces-
sary. It is to be supposed that early in phy-
logeny, increasing thickness of the shell
plates occurred with the result that a double
layered calcareous shell developed. This sit-
uation is also reflected to a certain degree in
the ontogeny of living chitons, where shell
formation begins with a calcium carbonate
secreting epithelium which later proliferates,
forming an epithelium of a perinotal aspect
with papillae now transformed into esthetes.

Kniprath (1979) interprets shell formation in
the Placophora, as Blumrich (1891) did ear-
lier, to be a simple lateral growth of perinotal
spines and he does not see any relevant dif-
ferences between perinotal spines and shell
plates. Accordingly, he does not accept any
homologies between the shell plates of the
Placophora and the shell of the Conchifera.
As а consequence, he denies the existence of
a properiostracal groove in the placophorans,
and he also cannot interpret the perinotum as
a mantle fold. He does not take into account
the above mentioned arguments which, pri-
marily on the basis of the number of the dor-
soventral muscles, support the hypothesis
that the concha of the Conchifera is a product
of the unification of the eight shell plates of the
Placophora. To argue that a simple lateral
growth of perinotal spines forms the shell
plates with accepting the argument that the
shell plates of the Placophora are in a phy-
logenetic connection with the concha of the
Conchifera is not consistent with the incor-
poration of the esthetes.

It could well be that the first shell formations
in chitons have been covered by the cuticle.
But this cuticle did not contain spines as
Beedham & Trueman (1967, 1968) proposed
in their reconstructions. As a consequence of
the origin of the placophoran shell plates from
the anlagen of spines or scales which corre-
spond to formations of the perinotum, it must
be concluded that the predecessors of the
Placophora possessed a mantle which corre-
sponded totally to the present placophoran
perinotum. These animals, which we wish to
call Archiadenopoda, must have been of a
chiton-like appearance but without plates.
They must have been covered by a mantle

HAAS

with calcareous spines or scales and with a
broad creeping foot. The eight shell plates in
Placophora (seven in Septemchitonida) are
the first acquisition of shells in the Mollusca.
After the formation of these shell plates in
Archiplacophora, the dorsoventral muscles
attached to them.

According to the fossil record, the Paleo-
zoic Placophora had posteriorly flattened con-
ical shell plates (Chelodes). (In general, a
cone seems to be the most primitive shape of
a shell with lateral and thickened growth.) The
supposed earliest chiton Matthevia from the
Upper Cambrian (Runnegar, Pojeta, Taylor
& Collins, 1979) with long conical shell plates
seems to be an extreme variant. If this animal
was indeed a chiton, the deep, mesially ar-
ranged holes in the inner shell must have
each contained a pair of dorsoventral muscles
diverging ventrolaterally to provide space for
the inner organs. The living chitons and most
of their fossil representatives have developed
clasp-like shell plates which are adapted to
the animal's life on hard substrata.

The question we have already discussed in
a previous section is the evolutionary direc-
tion of the well-established relationship of the
Placophora with the Solenogastres and
Caudofoveata. The concept that the Aplaco-
phora stem from the Placophora by loss of the
shell plates, advanced by Pelseneer (1890),
cannot be supported (Boettger, 1955) for we
only observe a reduction of the outer, but not
the inner, shell layer in certain taxa of rela-
tively high phylogenetic rank. From this it is to
be assumed that the Aplacophora never
possessed shell plates at all. Their ancestors,
which certainly must have been less highly
specialized than the living representatives of
the Solenogastres and Caudofoveata, must
be considered the predecessors of the Placo-
phora.

But in this context, the assumption that the
shell plates of the Archiplacophora have
formed directly from the transverse rows of
spiny scales of the Aplacophora (see Salvini-
Plawen, 1972) as they appear in the larvae of
the Solenogastre Nematomenia banyulensis
(Pruvot, 1890) must be rejected. Perhaps one
can interpret these conditions, as we have al-
ready discussed, as a pre-archiplacophoran
division into several areas of the dorsal man-
tle with respect to later shell plate areas. That
would mean that there is some vestige of the
predecessors of the Archiplacophora. It must
be said, however, that the observation of Pru-
vot (1890) needs reinvestigation. The above

EVOLUTION OF MOLLUSCAN CALCAREOUS HARDPARTS 417

reported speculations on the derivation of the
Placophora from the Aplacophora are sup-
ported by many of Salvini-Plawen’s (1972,
1980) arguments concerning the anatomy of
the soft body, and there is no contradiction
from the point of view of the calcareous hard
parts.

We can close our considerations with the
hypothetical Archiadenopoda and Archimol-
lusca (Salvini-Plawen, 1972, 1980) which
mainly represent stages in the evolution of the
molluscan foot. By these arguments the Cau-
dofoveata are the most primitive group next to
the Archimollusca.

From the concept of evolution of molluscan
calcareous hardparts, in all cases the most
primitive mollusc must have had a cuticle and
calcareous spicules or scales. Whether it had
a turbellarian ancestor as has been supposed
by various authors (Stasek, 1972, Stasek &
Williams, 1974; Salvini-Plawen, 1972, 1980)
or whether it was a preannelid (Boettger,
1955; Remane, Storch & Welsch, 1974; Sie-
wing, 1976) is still open to question. The pos-
session of calcareous spicules in certain tur-
bellarians (Rieger & Sterrer, 1975) has been
used by some authors (Runnegar, Pojeta,
Taylor & Collins, 1979; Salvini-Plawen, 1972;
Stasek, 1972; Stasek & McWilliamis, 1973) as
an argument for a turbellarian ancestor of the
molluscs. This conclusion is not yet convinc-
ing for these spicules are not situated in the
epithelium but underneath it. Their formation
is still unclear.

ACKNOWLEDGEMENTS

| thank my colleagues, Prof. Dr. N. Watabe
of the University of South Carolina at Colum-
bia, South Carolina and Prof. Dr. K. M. Wilbur
of Duke University, Durham, North Carolina
for reading the manuscript.

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INDEX TO SCIENTIFIC NAMES IN VOLUME 21
An asterisk (*) denotes a new taxon

abietina, Grammaria, 380
abyssalis, Utralvoherpia, 383
abyssicola, Limopsis, 89
abyssicola, Lyonsiella, 44
abyssorum, Xylophaga, 136. 143
Acanthinulinae, 157, 158
Acanthochitona, 388
Acanthogorgia, 383, 384
Acanthopleura, 406, 408, 409
Achatinacea, 157

aculeitecta, Sialoherpia, 383
Aculifera, 414

acuminata, Alexandromenia, 382
acuminata, Parapholas, 130, 136, 143
acuminata, Terebra, 365, 366, 368
acuta, Jullienia, 217, 218
adamsiana, Limopsis, 72
Adelopoma, 177

Adenopoda, 377, 386, 389, 396
aegypos, Teredo, 144

aequabilis, Falcidens, 374-377
affinis, Limopsis, 63, 68, 83, 84
affinis, Lyrodus, 144

affinis, Neomenia, 381

africana, Xylophaga, 130, 136, 143
agassizi, Anamenia, 383
aglaopheniae, Rhopalomenia, 379, 382, 385
alabastrina, Hydrobia, 261
alabastrina, Tomichia, 222

alatus, Euomphalopterus, 313
albiensis, Limopsis, 66, 71
Alcithoe, 285

Alcyonaria, 383, 384
Alexandromenia, 382

alfredensis, Barnea, 144

altenai, Xylopholas, 130, 136, 143
amandae, Limopsis, 71
Amberleya, 335, 336
Amberleyacea, 292, 293, 311, 330, 334, 335
Amberleyidae, 335

Amberleyinae, 335

americanus, Spondylus, 27, 32
Amphidromus, 175
Amphimeniidae, 385
Amphiscapha, 313, 315, 317, 320
Amphitomaria, 314

Ampullariidae, 315, 323

Amusium, 23, 27, 28

anacarina, Turbinilopsis, 316
Anamenia, 379, 383, 385

anatina, Laternula, 42

Anculosa, 211

Ancylus, 12

anechoensis, Bankia, 144
Angaria, 336

angasi, Offadesma, 41, 42, 44, 53
angustiflora, Acanthogorgia, 383, 384
Anisostoma, 314, 334, 335
annulata, Dondersia, 380
Anomalodesmata, 35-60, 391

Anomia, 29

Anomiacea, 23, 24, 26, 27, 31

Anomphalacea, 292, 311, 314, 330, 333

Anomphalidae, 333

anserifera, Laternula, 42

antarctica, Alexandromenia, 382

antarctica, Gephyroherpia, 381

antennina, Nemertesia, 381

Anthozoa, 381

antillensis, Limopsis, 62, 73, 89

aperta, Tricula, 215, 216, 218, 220, 222

Aplacophora, 371, 377, 401, 403, 412, 415—417

Aquidauania, 211, 212, 221

Arca, 62

Arcacea, 62, 72

Archaeogastropoda, 170, 291-336, 353, 354, 359-
361, 393, 394

Archaeomenia, 379, 380

Archaicinae, 150

Architaenioglossa, 361

Architectonicidae, 285, 315, 317, 368

Arcidae, 72, 75

Arcoidea, 61-93

arctatum, Mesodesma, 96, 97, 101, 102, 104, 107,
108

arechavalettoi, Mesodesma, 96

argenteum, Chaetoderma, 376

Ariantinae, 150

Arionidae, 157, 158

Ariophantacea, 157

Ariophantidae, 157, 158, 164

armata, Acanthogorgia, 383, 384

Armenica, 162

Arthrocnemum, 232

Arthropoda, 384

Asaphis, 104

Aspella, 268

Aspidobranchia, 359

Aspidopholas, 117, 144

Assiminea, 225, 233, 261

Asthenothaerus, 41

Atactodea, 96, 105, 107

atlantica, Rhopalomenia, 382

atlantica, Xylophaga, 122, 130, 136, 143

atriolonga, Genitoconia, 380

augustae, Limopsis, 71, 75

Aulacopoda, 157, 158

aurita, Limopsis, 62, 66, 67, 69, 71, 74, 83-85

aurita, Xylophaga, 136, 143

australasiae, Barnea, 144

australis, Bankia, 130, 133, 144

australis, Epimenia, 384

Australonema, 333

austrina, Phyllomenia, 381

Autobranchia, 391

azorica azorica, Leptaxis, 175

bacillum, Chaetoderma, 376

Bactronophorus, 117, 123, 130, 133, 134, 137, 143

Balcis, 284

Balea, 169

(419)

420 MALACOLOGIA

Bankia, 111-148

Bankiinae, 115-117, 124, 127, 134, 138, 139, 144

banyulensis, Nematomenia, 379, 380, 416

Barnea, 115, 117, 130, 135, 136, 138, 143, 144

barthelowi, Bankia, 144

bartschi, Teredo, 112, 116-122, 138-141, 144

bassi, Limopsis, 65, 69, 88, 90, 93

basteroti, Terebra, 364, 365

bathonica, Amberleya, 335

Bathyarca, 69

Bathybembix, 335

bavayi, Pachydrobia, 215

belcheri, Limopsis, 62, 81

Bellatara, 283

Bellerophontacea, 296, 314, 323

Beraunia, 313, 315, 316

bicallosa, Perforatella, 151

binneyi, Pomatiopsis, 239

bipalmulata, Bankia, 144

bipartita, Lyrodus, 144

bipennata, Bankia, 144

Birasoherpia, 383

birmanica, Barnea, 144

bitubulatus, Triforis, 368

Bivalvia, 23-34, 61-93, 95-110, 371, 387, 390,
391, 393-397

Blanfordia, 211, 212, 221, 239

Boettgeria, 169

bollingi, Tricula, 215, 222

borealis, Anamenia, 283

boschasina, Laternula, 42

*boucheti, Palaina, 179, 182, 185-192, 195-198,
201, “202, 203

bracteata, Lyratoherpia, 380

Bradybaena, 173

Bradybaenidae, 150, 157, 158, 163, 164, 172, 174,
175

branchiata, Parapholas, 136, 143

brandti, Paraprosothenia, 217

brazieri, Limopsis, 70, 72, 74, 92, 93

Brechites, 36, 43, 52, 57

brevis, Bankia, 144

brevis, Pachydrobiella, 217, 218

Brochidium, 334

bruuni, Xylophaga, 136, 143

Bryozoa, 388

Buccinacea, 368

Bulimulidae, 172, 175

Bulinus, 233, 234

burchi, Tricula, 222

Burmesiidae, 50, 54

Burnupia, 234

Bythograea, 307

Caecella, 95, 101, 102, 104, 106, 108

Caenogastropoda, 353

caldeirarum, Leptaxis, 175

Calicogorgia, 383

californica, Parapholas, 130, 136, 143

californicum, Chaetoderma, 376

californicum, Prochaetoderma, 375, 376

Calliostoma, 315, 359

Calliotropis, 335

calva, Parapholas, 136, 143

Calyptogena, 292

Calyptraea, 211, 214, 220, 358

Calyptraeacea, 355, 358

Calyptraeidae, 211, 284, 286, 291-336

Camaenidae, 175

campanellata, Bankia, 130, 133, 144

Campanile, 263-289

Campanilidae, 263-289

Campanilopa, 280, 281, 283

Campanilinae, 280

Campanulariidae, 380

campechiensis, Pholas, 130, 136, 143

canadense, Chaetoderma, 375-377

canaliculata, Pomacea, 361

Canariella, 168

cancellata, Limopsis, 62, 90

candida, Barnea, 130, 136

candida, Pholadomya, 36, 45, 46, 48-57

Candidula, 151

capensis, Burnupia, 234

Cardiomya, 51

Carditacea, 73, 75

carinata, Bankia, 144

carinata, Lyratopherpia, 380

carinata, Neomenia, 379, 381

carinata, Rhopalomenia, 382

carinata, Sandalomenia, 380

Caucasotachea, 162

caudatus, Falcidens, 375, 376

Caudofoveata, 371-375, 393, 395-397, 400, 401,
403, 412-414, 416, 417

Cavibelonia, 381, 396

cawstoni, Tomichia, 221, 222, 225, 230, 234, 261,
262

Cecina, 211, 212, 221

ceiba, Bankia, 144

centrifuga, Serpulospira, 313

Cepaea, 151

Cephalopoda, 291, 321, 371, 372, 387, 390, 392,
394400

Ceratomyacea, 55

Ceratomyopsidae, 50

Ceratopea, 331

Ceratophallus, 234

Ceratoptilus, 280, 281

Cerion, 2

Cerithiacea, 263-289

Cerithiidae, 280, 285-287

Cerithiopsidae, 286, 287

Cerithium, 280-282, 285

Cernuella, 150, 151

Cetoconcha, 51

Chaceia, 117, 130, 135, 136, 143

Chaenomyidae, 50

Chaetoderma, 373-377, 401

Chaetodermatidae, 373-376, 397, 400

Chaetodermatina, 371

chamaeleon, Paramuricaea, 383

Chamidae, 37, 38

Chara, 234

Chelodes, 416

cheveyi, Aspidopholas, 144

chiloensis, Pholas, 130, 136, 143

INDEX TO VOL. 21 421

chinensis, Caecella, 101, 102, 104, 106, 108

Chlamys, 25-29

Chondrinidae, 157, 158

Chondrulinae, 157, 158

chuni, Limopsis, 80, 81

Cidarina, 335

cincinnatiensis, Pomatiopsis, 232

cinerea, Lepidochitona, 388, 405, 407, 408, 410-
412

Cionellacea, 157

Cionellidae, 157, 158

Cirridae, 313, 335

Cirrus, 335, 336

clappi, Lignopholas, 136, 143

clappi, Teredo, 130, 133, 144

Clausiliacea, 157

Clausiliidae, 157-162, 164, 169, 171, 174, 175

Clausiliinae, 157, 158, 161, 162

Clavagella, 36, 43, 52

Clavagellacea, 35, 36, 42-44, 48, 50, 52-57

Clavagellidae, 36, 42-44, 50, 54, 56, 57

clavus, Uperotus, 130, 133, 134, 144

Cleidothaeridae, 36-40, 50, 52-54, 56

Cleidothaerus, 36, 38, 40, 53, 56

clenchi, Xylophaga, 136

Clisospira, 331

Clisospiracea, 292, 311, 330, 331, 334

Clisospiridae, 331, 332

Cnidaria, 371, 379-385, 388, 396, 397, 400

cnidevorans, Dondersia, 380

Cocculina, 325

Cocculinacea, 325

Cocculinidae, 296

Cocculinoidea, 325

cochleata, Mimospira, 331

Cochlicella, 151, 174

Cochlicopidae, 157

Cochlodesma, 39, 41, 49, 53

Cochlodininae, 157, 158

Cochlostomatidae, 177

Cochlostomatinae, 181, 182

Codonocheilidae, 334

coemansi, Limopsis, 66, 71

Coleoida, 392, 393

communis, Acanthochitona, 388

compacta, Lecanospira, 324

compacta, Montacutona, 55

complanata, Mesodesma, 103

complex, Dichostasia, 335

compressa, Limopsis, 90

concava, Xylophaga, 136, 143

Conchifera, 371, 389, 390, 393, 395-397, 400,
403-418

Concholepas, 310

conica, Lacunopsis, 218

conicum, Microdoma, 333

conicus, Hipponix, 279

conradi, Penitella, 130, 136, 143

conspurcata, Xerotricha, 174

convexa, Xylophaga, 130

copulobursata, Rhipidoherpia, 379, 384

corallensis, Limopsis, 71

Coralliophilidae, 314

Corallium, 380

corallophila, Nematomenia, 380
Corbicula, 139

Corbula, 97

cornea, Mesodesma, 98
cornuadentata, Phyllomenia, 381
coronata, Hubendickia, 217, 218
coronata, Lacunopsis, 214
coronatum, Oriostoma, 313
corrugata, Terebra, 365, 366, 368
Corynidae, 382

Cosa, 75

costata, Cyrtopleura, 130, 136, 143
costata, Jullienia, 217, 220
costulata, Hastula, 364, 366-368
Coxiella, 209, 211, 212, 221, 238
Craspedopomatinae, 170
Craspedostoma, 334-336
Craspedostomatacea, 291-336
Craspedostomatidae, 334
Crassostrea, 99, 108

Cratis, 62, 75

crenagulata, Neomenia, 381
Crepidula, 303

crispata, Zirfaea, 136, 143
cristata, Limopsis, 63, 68, 71, 83
cristata, Rhopalomenia, 382
crooki, Hubendickia, 217

crooki, Jullienia, 217

crooki, Pachydrobia, 215
Crossostomatidae, 334
crossotus, Falcidens, 374-377
cruciger, Cyrtopleura, 130, 136, 143
Crustacea, 75

cryophila, Pruvotina, 382
Cryptolaria, 382

Crysogorgiidae, 384
Ctenidiobranchia, 391

cumingi, Limopsis, 67, 82, 83
cumingiana, Caecella, 106, 108
cumingi, Jouannetia, 136, 143
cuneiformis, Martesia, 136, 143
curta, Diplothyra, 136, 143
Cuspidaria, 45, 50, 51, 56
Cuspidariacea, 35, 54-57
Cuspidariidae, 36, 38, 44, 45, 47, 49-52, 54, 56, 57
cuspidata, Cuspidaria, 51
Cycas, 184

“Cyclonema,” 333

Cyclopecten, 27, 28
Cyclophoracea, 177, 180, 181, 360, 361
Cyclospongia, 316

cylindrica, Hubendickia, 218
Cylindropalaina, 180, 200
Cylindrus, 151, 175

Cypraeacea, 284

Cyrtodontidae, 75

Cyrtopleura, 117, 130, 134-136, 143
dactylus, Pholas, 130, 136, 143
dalli, Limopsis, 81

dalyelli, Neomenia, 381

Danilia, 334, 335

dannevigi, Limopsis, 93

422 MALACOLOGIA

darwini, Nettastomella, 136, 143 Endodontidae, 157, 158, 168, 169
Daudebardiinae, 157, 158 Enidae, 157-159, 169-171, 174, 175
davisi, Karelainia, 216-218 Eninae, 157, 160, 164

debilis, Strophomenia, 383 Enigmonia, 24

decussata, Nipponolimopsis, 67, 71 Ensis, 97

Delavaya, 212, 216 ensis, Ensis, 97

Dendronephthya, 383, 384 entale, Dentalium, 392
Dendropoma, 284 Entodesma, 36, 37

Dentaliida, 392 Entomostraca, 379, 383
Dentalium, 392 epibionta, Proneomenia, 384
destructa, Bankia, 144 Epimenia, 384, 385, 401

Dialidae, 286 Epizoanthus, 383

Diastomidae, 286, 287 erecta, Xylophaga, 136, 143
diazi, Limopsis, 83 erosa, Geloina, 52

Dichostasia, 334, 335 erosa, Polymesoda, 52
dichotoma, Asaphis, 104 eruditum, Chaetoderma, 375, 376
Dicyathifer, 117, 123, 130, 133, 134, 137, 143 Euciroa, 50

diegensis, Limopsis, 63, 68, 83, 84, 86 Euconulidae, 157, 158

differens, Tomichia, 209-262 eucosmus, Limopsis, 65, 69, 72, 90, 93
dilatata, Barnea, 144 Euomphalacea, 291-336
Dimyidae, 23 Euomphalidae, 312-314, 317, 323
Dinomenia, 382 Euomphaliinae, 150

Diodora, 353, 358 “Euomphalina, 292, 293, 312, 324, *325
Diozoptyxis, 282 Euomphalopteridae, 312, 313
Diplommatina, 177, 178, 180, 199, 203, 204 Euomphalopterus, 313, 314
Diplommatinidae, 177-208 Euomphalus, 284, 313, 317
Diplommatininae, 177, 182 Euthyneura, 283

Diplothyra, 117, 130, 135, 136, 143 ewingi, Neopilina, 389
Dirocerithium, 283 ewingi, Vema, 389

Discinae, 157, 158 exacuminata, Hastula, 364, 367
Discohelix, 314 excavata, Teredothyra, 143
Discula, 151, 175 eximia, Poromya, 50

Discus, 169 expansa, Halewisia, 215, 218
docens, Beraunia, 313 explanata, Talona, 130, 136, 143
dominicensis, Teredothyra, 130, 133, 143 Falcidens, 374-377, 413

Donax, 96, 101-105, 107, 108 farcimen, Anamenia, 383
Dondersia, 380 farinesi, Hastula, 364, 366-368
Dondersiidae, 401 fascicularis, Acanthochitona, 388
dorsalis, Xylophaga, 122, 130, 136, 143 Fenouilia, 216

dorsosulcata, Hemimenia, 381 Ferussaciidae, 157, 158, 169
Dorymenia, 379, 384, 385 Ficidae, 368

Drepanomenia, 383 Ficus, 368

Drosophila, 221, 239 fimbriatula, Bankia, 111, 112, 117-121, 144
drouetina, Leptaxis, 175 fischeriana, Pachydrobia, 215
dryas, Nausitora, 144 fischerpietti, Lacunopsis, 214, 220
duchassaingi, Jouannetia, 130, 136, 143 fissitubata, Sputoherpia, 383
dumosa, Lafoea, 380 Fissurellacea, 354

dunlopei, Nausitora, 130, 133, 144 Fissurellidae, 296, 304, 391, 395
duplicata, Xylophaga, 136, 143 fitchi, Penitella, 130, 136, 143
duryi, Helisoma, 408 flavens, Nematomenia, 380
Ecologarinia, 180 flexuosa, Halicardia, 50

edax, Nototeredo, 130, 133, 144 floridana, Lyrodus, 112, 118-121, 130, 133, 138,
Edmondiidae, 50 139, 144

elachista, Limopsis, 64, 68, 71 fluminea, Corbicula, 139
Eledone, 392 fluviatilis, Ancylus, 12

elegans, Hydrorissoia, 217, 218 fodiens, Micromenia, 379
elephantina, Odontomaria, 324 foliata, Xylophaga, 136, 143
Eleutheromenia, 381, 385 Foraminifera, 392

elliptica, Laternula, 42 forbesianus, Hemipecten, 23-34
elongatus, Psilodens, 373, 376 Forcepimenia, 382

emarginata, Thais, 12 formosa, Lyonsiella, 45, 47, 51
enderbyensis, Limopsis, 93 forskali, Limopsis, 90

Endodontacea, 157 forteradiata, Limopsis, 69, 90

INDEX TO VOL. 21

Fossarus, 216, 217

fosteri, Bankia, 144

foveatus, Fossarus, 216, 217
fragilis, Barnea, 144

fragilis, Lyonsiella, 44, 45, 47, 50, 51
fragilis, Martesia, 130, 136, 143
fragilis, Parilimya, 46, 47, 49-51, 55
*fretterae, Neomphalus, 291-*294-361
fruticum, Bradybaena, 173

fucifera, Teredo, 130, 133, 144
Fukuia, 211, 212, 221

fulleri, Teredo, 133, 144

fuscata, Terebra, 364-366, 368
fusticula, Nausitora, 130, 133, 135, 144
gabbi, Penitella, 130, 136, 143
gaederopus, Spondylus, 32
galatheae, Neopilina, 389, 390
galatheae, Xylophaga, 136, 143
Galeroconcha, 371, 388-390
Gastrocoptinae, 163
Gasterodontinae, 157, 158

Gastropoda, 5-13, 263-289, 291-361, 363-369,

371, 387, 390, 391, 393-397, 400
Geloina, 52
Genitoconia, 380
Geomitrinae, 150, 151, 153, 154, 158, 168, 170,
171
Gephyroherpia, 381
gerda, Xylophaga, 136
Gersemia, 383
gerstfeldti, Perforatella, 151
giganteum, Campanile, 264, 268, 280
giganteum, Cerithium, 281
gigas, Campanile, 282
gigas, Cerithium, 281
gigas, Ostrea, 108
gigas, Telescopium, 280
glabrata, Atactodea, 105, 107
globosa, Jouannetia, 130, 136, 143
globosa, Lacunopsis, 214
globosa, Xylophaga, 122, 136, 143
Glycymerididae, 61, 62, 74
Glycymeris, 62, 69
glycymeris, Glycymeris, 62
gochenouri, Hubendickia, 218
gomphoceras, Campanile, 282, 283
Gorgonaria, 382-384
gorgonophila, Anamenia, 379, 383, 385

gouldi, Bankia, 111, 112, 117-122, 127, 130, 133,

139, 140, 144
Gourmya, 285
gourmyi, Gourmya, 285
gowllandi, “Eclogarinia,” 180
gracilis, Bankia, 144
gracilis, Hydrorissoia, 217
Grammaria, 380, 382
Grammysidae, 50
granulata, Acanthopleura, 406, 408, 409
granulata, Poromya, 47
grevei, Xylophaga, 136, 143
guineensis, Xylophaga, 144
Guianadesma, 35, 53, 55
gutta, Hydrocena, 170

gutturosus, Falcidens, 375-377, 413
Gymnomorpha, 393

Gymnosomata, 396

hadalis, Xylophaga, 136, 143
Halewisia, 210-212, 215, 218
Halicardia, 50

Haliotidae, 296

Haliotis, 35

Hanleya, 388, 409

hanleyanus, Donax, 96, 101-104, 107
hanleyi, Hanleya, 388

hanseni, Paraprososthenia, 216, 217
harmandi, Jullienia, 217, 218
harmandi, Lacunopsis, 214, 220
harpagata, Dorymenia, 384
harpagata, Lepidomenia, 380
hartmani, Falcidens, 375

Hastula, 364, 366-368

hawaiiense, Chaetoderma, 376
healdi, Psiloterdeo, 130, 133, 140, 144
Heathia, 380

hedleyi, Nausitora, 130, 133, 144
helenae, Limopsis, 71

Helicacea, 157

Helicella, 150

Helicellinae, 149-176

Helicidae, 149-176

Helicigoninae, 150-153, 155, 158

423

Helicinae, 150, 151, 153, 155, 158, 162, 168

Helicodontidae, 150

Helicodontinae, 150, 151, 153, 155, 158, 168

Helicoidea, 150

Helicopsis, 150
Helicostylinae, 175
Helicotoma, 314, 324
Helicotomidae, 314
Helisoma, 408

Helix, 153, 169

Helixena, 151, 174, 175
Hemicycla, 168, 171
Hemimenia, 379, 381
Hemipecten, 23-34
hendrickxi, Hydrobia, 233, 234
herwigi, Neomenia, 381
Heterodonta, 115
Heteropoda, 371, 391, 395
Heterurethra, 157, 158
Hexacorallia, 380-383
Hinnites, 23, 26, 27, 31, 32
Hippocampoides, 314
Hipponicacea, 358
Hipponix, 279

hirondellei, Meromenia, 383
hirtella, Limopsis, 93
hoeninghausii, Limopsis, 66, 71
hoffmani, Dorymenia, 384
Holopea, 333

Holopeidea, 333

Holopoda, 157, 158
Holopodopes, 157, 158
horrida, Laevicordia, 47
hortensis, Cepaea, 151
hospitalis, Hydrorissoia, 218

424 MALACOLOGIA

Hubendickia, 209-262

hubrechti, Dinomenia, 382

humilior, Palaina, 200

Humphreyia, 43

hupensis, Oncomelania, 218, 230, 239
hyalina, Neopilina, 389

hyalina, Vema, 389, 390

Hydrobia, 209-262

Hydrobiidae, 218, 222, 236
Hydrobiinae, 218

Hydrocena, 170

Hydrorissoia, 211, 212, 216-218, 230
hydrorissoidea, Karelainia, 217
Hydrozoa, 380, 382, 384
Hygromiidae, 150

Hygromiinae, 150, 151, 153, 155, 158-160, 162-

164, 174
Hypomenia, 382
Hystricella, 151
idonea, Limopsis, 83
llaira, 334
Imeroherpia, 381
impexa, Pruvotina, 378
inaequivalvis, Pandora, 37, 38, 55
incerta, Pachydrobia, 215
indica, Limopsis, 81, 83
indica, Strophomenia, 379, 383, 385
indica, Xylophaga, 136, 143
infundibulum, Lesueurilla, 324
ingolfia, Xyloredo, 130, 136
Inoceramidae, 75
inornata, Barnea, 144
insperata, Danilia, 335
intergenerica, Syngenoherpia, 384
intermedia, Hemimenia, 379, 381
intermedia, Limopsis, 83
intermedium, Chaetoderma, 375, 376
Isognomostoma, 150, 164
Jaminiinae, 157, 158
janeiroensis, Limopsis, 81, 83
Janulus, 169
japonica, Acanthogorgia, 383
japonica, Nettastomella, 130, 136, 143
japonica, Xylophaga, 144
japonicum, Chaetoderma, 376
johnsoni, Teredo, 144
Jouannetia, 117, 124, 130, 135, 136, 143
Jouannetiinae, 117, 123, 124, 126, 127, 143
juarezi, Limopsis, 86
Jullienia, 211, 212, 216-218, 220
Jullieniini, 210-212, 214-218, 222
Karelainia, 211, 212, 216-218, 222
kearneyi, Palaeotrochus, 333
Kelliella, 392
knockeri, Hastula, 366
knoxi, Nototeredo, 130, 133, 144
knudseni, Xylophaga, 144
*kuniorum, Palaina, 186-190, 200, “204
Kuphinae, 112, 115-117, 124, 126, 127, 143
Kuphus, 111-148
Labidoherpis, 382
labrosa, Neomenia, 381
lacazei, Strophomenia, 383

Lacunopsini, 210-212, 214, 215, 218
Lacunopsis, 211, 212, 214, 218, 220
laeve, Cerithium, 218, 282

laeve, Pyrazus, 282

laeve, Telescopium, 282
Laevicordia, 47

laevis, Ceratoptilus, 282

laevis, Straparollus, 313, 317

Lafoea, 380

Lafoeidae, 382

Lambis, 287

Lamellaria, 306

Lamellibranchia, 391

lamellosa, Barnea, 130, 136, 143
lamellosa, Thais, 12

laminata, Dondersia, 380

laminata, Neomenia, 381

lanceolata, Cyrtopleura, 130, 136, 143
lanceolata, Limopsis, 83

Lanistes, 315, 323, 332

lapidaria, Pomatiopsis, 230, 232, 249
lata, Limopsis, 89

Laternula, 42, 53

Laternulidae, 36, 39-42, 49, 50, 53-56
latosoleata, Alexandromenia, 382
laxopharyngeata, Sputoherpia, 383
Lecanospira, 323, 324, 331
Leiostyla, 169

Lejeania, 151

Lepetellacea, 325

lepida, Hastula, 364, 366-368
Lepidochitona, 388, 405, 407, 408, 410—412
Lepidomenia, 380

Lepidopleuridae, 387, 388
Leptaxinae, 150-153, 158, 168, 170, 174
Leptaxis, 175

Leptonacea, 55

Lesueurilla, 292, 314, 323, 324
Levantina, 162

levayi, Paraprososthenia, 217

leve, Cerithium, 280, 282

Lignopholas, 115, 117, 124, 130, 134-136, 140,

143
lilliei, Limopsis, 65, 70, 72, 73, 75, 82, 91, 93
lilydalensis, “Cyclonema,” 333
Limacidae, 157, 158
Limidae, 26, 46
Limifossor, 373, 375, 376
Limifossoridae, 374, 376
Limnoria, 111
Limopsacea, 73
Limopsidae, 61-93
Limopsis, 61-93
Lindholmiolinae, 150
linsa, Sallya, 333
Liomphalus, 314-316
liosqameus, Falcidens, 377
lirata, Assiminea, 225, 261
Liotia, 336
Liotiidae, 292, 314, 317, 334-336
Liotiinae, 334
lirata, Tomichia, 225
lissa, Hastula, 367

INDEX TO VOL. 21 425

Lithoglyphopsis, 212, 215

Litiopidae, 286

Littorina, 211, 220

Littorinacea, 335

Littorinidae, 211, 215, 285

lituifera, Ocheyoherpia, 381

Lituiherpa, 381

lobata, Xylophaga, 136, 143

logani, Maclurites, 331

Loligo, 392, 393

longipilosa, Limopsis, 83

longispinosa, Pruvotina, 381

Lophomenia, 382

loringi, Limopsis, 62, 65, 69, 70, 72, 73, 90, 93

loscombiana, Pholadidea, 106, 108, 130, 136, 143

lubbocki, Weeksia, 313

Lutraria, 95, 101

lutraria, Lutraria, 101

Lymnaea, 5-13

Lyonsia, 36, 37, 44, 52

Lyonsiella, 44, 45, 47, 50, 51

Lyonsiellidae, 36, 51

Lyonsiidae, 36-39, 53-56

Lyratoherpia, 380

Lyrodus, 111-148

Lytocarpia, 380-382

mabillana, Limopsis, 83

macgillivrayi, Limopsis, 90

macgillivrayi, Palaina, 178, 180

Macluritacea, 291-336

Maclurites, 330, 331

Macluritida, 318

Macluritidae, 313, 323, 331

Macluritina, 293, 310, 325

Macluritoidea, 325

Macropalaina, 180, 210, 204

Mactra, 95, 101, 106-108

Mactracea, 95

Mactridae, 56, 104

mactroides, Mesodesma, 95-110

mactroides, Tivela, 98, 103, 107

maggae, Limopsis, 72

Magilinidae, 314

magnifica, Calyptogena, 292

malleolus, Teredora, 130, 133, 144

Malleus, 24

manilensis, Barnea, 144

manni, Dicyathifer, 130, 133, 143

maorianus, Cleidothaerus, 40

*mareana, Palaina, 182, 186-190, 200, 204, 205,
*206, 207

Margaritariidae, 50

Margarites, 311

mariei, Cylindropalaina, 200

mariei, Diplommatina, 200

mariei, Palaina, 177-208

marionensis, Limopsis, 62, 63, 67, 74, 80, 81

martensi, Bankia, 144 :

Martesia, 111-148

Martesiinae, 111-148

massa, Lyrodus, 130, 133, 134, 144

massei, Lacunopsis, 214, 220

Matthevia, 416

matocotana, Teredothyra, 130, 133, 143

maximus, Pecten, 26, 28

medilobata, Lyrodus, 130, 133, 144

mediterranea, Corbula, 97

Megadesmidae, 50

megaradulata, Sputoherpia, 383

Megaspiridae, 175

megathecata, Pruvotina, 381

megotara, Psiloteredo, 127, 130, 133, 134, 144

melanoides, Neodiastoma, 287

melanura, Pholadidea, 130, 136, 143

mera, Mactra, 106-108

Meromenia, 383

mesenterina, Turbinaria, 29

Mesodesma, 95-110

Mesodesmatidae, 95-110

Mesogastropoda, 170, 180, 209-263, 284, 286,
292, 310, 323, 353-355, 359-361, 390, 394

Mesurethra, 157, 158

Metachaetoderma, 373, 395

Metafruticicolinae, 150

Metamenia, 382

mexicana, Xylophaga, 136, 143

micans, Hastula, 366

Microdoma, 333

Microdomatacea, 292, 311, 330, 333

Microdomatidae, 333

Micromenia, 379, 380

microps, Limopsis, 72

Milacidae, 157, 158

militare, Chaetoderma, 377

Mimospira, 331, 332

mindanensis, Teredo, 144

minima, Limopsis, 66, 70, 71

minima, Oncomelania, 239

minor, Leptaxis azorica, 175

minuta, Limopsis, 63, 64, 68, 69, 87-89

misjae, Limopsis, 71

modesta, Terebra, 364, 365

Modiolidae, 75

Modiomorphacea, 75

Modulidae, 285, 286

Mollusca, 1—4, 371-418

Monacha, 150, 153, 155, 158

“Monachines,” 150

Monilearia, 168, 171

Monodonta, 357

Monoplacophora, 321, 388-390

Monostichoglossa, 385

Monotocardia, 323, 355, 361

Montacutona, 55

montereyense, Chaetoderma, 375, 376

montrouzieri, Diplommatina, 199

montrouzieri, Palaina, 181, 182, 185-196, 198-
201, 204, 205

Mopalia, 388

Mopaliidae, 388

multirugosus, Hinnites, 27, 31, 32

multistriata, Limopsis, 65, 69, 82, 88, 89, 90

munensis, Jullienia, 217

Murchisonioidea, 325

Murella, 151

Muricacea, 383

426 MALACOLOGIA

muroaki, Xylophaga, 136

murrayi, Xylophaga, 136, 143

mutabilis, Strombus, 287

Mya, 15

Myadora, 37-39, 52

Myochama, 36, 37, 52

Myochamidae, 36-40, 52-54, 56

Myoida, 115

myriophyllum, Lytocarpia, 380-382

Mytilacea, 23-25

Mytilidae, 75, 293, 309

Mytilimeria, 37

Mytilus, 15, 19

naceli, Xyloredo, 136, 143

nanae, Limopsis, 71

*nanodes, Palaina, 182, 187-190, “203

nanulum, Chaetoderma, 376

Napaeinae, 157, 158, 170

Napaeus, 169, 174, 175

natalensis, Ceratophallus, 234

natalensis, Tomichia, 209-262

natalis, Limopsis, 64, 87, 89

Nausitora, 116, 117, 123, 130, 133-135, 140, 144

Nautiloidea, 321

Nautilus, 392, 393

navalis, Teredo, 112, 117-122, 127, 130, 133, 144

Nematomenia, 379, 380, 416

Nemertesia, 381

Nemertini, 395

Neobankia, 116

Neodiastoma, 287

Neogastropoda, 263, 286, 310, 371, 390, 391, 394—
396

Neolepas, 321

Neoloricata, 404

Neomenia, 379, 381

Neomeniamorpha, 380

Neomeniina, 371

*Neomphalacea, 292, 293, *294, 312, 324

*Neomphalidae, 292, *294, 309, 320-322

*Neomphalus, 291-*294-361

Neopilina, 137, 372, 389, 390, 393-396, 415

Neopilinidae, 321

Neoteredo, 117, 123, 127, 130, 133, 134, 137, 143

Neotrigonia, 287

Nephthya, 384

Nerineidae, 282, 283

Neritacea, 292, 323, 330, 359, 361

Neritidae, 215, 296, 316

Neritina [suborder], 325

Neritopsina, 390, 393

Nettastomella, 117, 124, 130, 134-136, 143

Nevadispira, 317

neztalia, Bankia, 144

nierstraszi, Hypomenia, 382

niphas, Leptaxis, 175

nipponense, Halicardia, 50

Nipponolimopsis, 67, 71

Nipponopanacca, 46, 47

“nissidiophila, Palaina, 182, 186-193, 195, 196,
198, 201—203

nitidulum, Chaetoderma, 374-376

Nododelphinulidae, 335, 336

Noetiidae, 72

nooi, Xyloredo, 136, 143

nordenskioldii, Zenobiella, 151

northi, Liomphalus, 315, 316

norvagica, Nototeredo, 127, 130, 133, 144

norvegica, Lyonsia, 36, 37

Nototeredo, 116, 130, 133, 134, 138, 144

novaezelandiae, Mesodesma, 103

nucula, Jullienia, 217

Nuculidae, 371, 391, 395

nuttalli, Schizothaerus, 107

obesa, Diplommatina, 201

obesa, Macropalaina, 201

obesa, Palaina, 186-190, 196, 201, 202

obliqua, Limopsis, 83

oblonga, Limopsis, 68, 70, 84, 87

obtecta, Aspidopholas, 144

obturamentum, Barnea, 144

obtusa, Spathoteredo, 130, 133, 144

obtusa, Xylophaga, 136

obtusata, Xylophaga, 143

obtusus, Cylindrus, 151, 175

Ocheyoherpia, 381

Octobrachia, 392

Octocorallia, 379, 383, 394

Octopus, 393

Odontomaria, 314, 324

Offadesma, 41, 42, 44, 53, 55

Oleacinacea, 157

Oleacinidae, 157, 158

oligotropha, Neopilina, 390

Omphalocirridae, 312-314, 316, 317

Omphalocirrus, 313, 331

Omphalotrochidae, 312-315, 323

Omphalotrochus, 313, 316

Onchidella, 390, 393

Oncomelania, 211, 212, 218, 221, 230, 239, 254

Onychochilidae, 331, 332

Onychochilus, 331, 332

oolithica, Limopsis, 66, 70

*opaoana, Palaina, 182, 185-192, 195-198, 200,
201, 204-*205-206

opercularis, Chlamys, 28

operculata, Cryptolaria, 382

ophidiana, Strophomenia, 384

Opisthobranchia, 310, 394

Opisthostoma, 182

Orculidae, 157, 158, 163

orcutti, Bankia, 144

orientalis, Pholas, 144

Oriostoma, 313, 314, 316

Oriostomatacea, 311, 330

Oriostomatidae, 312-317, 323

Orthurethra, 158

Ostracoda, 392

Ostrea, 15, 74, 108

Ovalarca, 72

ovoidea, Chaceia, 130, 136, 143

Oxychilus, 169

Ozaena, 392, 393

Pachydrobia, 210-212, 215, 216, 218, 220, 236

Pachydrobiella, 211, 212, 216-218

pachyptila, Riftia, 292, 307

INDEX TO VOL. 21 427

pacifica, Euciroa, 50 perroquini, Palaina, 180, 182, 186-190, 204, 205
Paedhoplitinae, 150 perticata, Drepanomenia, 383
Palaeobranchia, 391 Petaloconchus, 284

Palaeotaxodonta, 50, 54 Phaedusinae, 157, 158, 161
Palaeotrochacea, 292, 311, 330, 333 phaseolina, Thracia, 39-41
Palaeotrochidae, 333 Phasianellidae, 296, 311

Palaeotrochus, 333 Phenacolepadidae, 296

Palaina, 177-182, 185-207 philippi, Bankia, 144

pallioglandulata, Pruvotina, 381 Philippia, 368

Paludina, 225 Philobrya, 75

Panacca, 46, 47 Philobryidae, 61, 62, 71, 75

panamensis, Limopsis, 86 Pholadacea, 111-148

panamensis, Uperotus, 130, 144 Pholadidae, 111-148

panamensis, Xylophaga, 136, 143 Pholadidea, 106, 108, 117, 130, 135, 136, 143
Pandanus, 178 Pholadina, 115

Pandora, 37, 38, 55 Pholadinae, 117, 126, 138, 143
Pandoracea, 35-39, 42, 44, 50, 52-57 Pholadomya, 36, 45-57

Pandoridae, 36-39, 50, 54, 56 Pholadomyacea, 35, 36, 45—48, 50, 52, 53, 55-57
Papuininae, 175 Pholadomyidae, 45-49, 53, 56
paradoxa, Limopsis, 81 Pholadomyoida, 35, 36, 50, 56
Paragalerus, 309 Pholas, 117, 130, 135, 136, 143, 144
Paramuricaea, 383 Pholidoskepia, 380, 401

Parapholas, 117, 130, 135, 136, 143, 144 Phyllomenia, 381

Paraprososthenia, 211, 212, 216, 217 physa, Onychochilus, 331

Parapyrgula, 212, 216 pilsbryi, Zirfaea, 130, 136, 143
Pararhytida, 203 Pinctada, 23, 24

Parilimya, 36, 45-47, 49-53, 55-57 Pinnacea, 75

Parilimyidae, 45, 47, 50, 56 pisana, Theba, 174

parksi, Teredo, 144 Placiphorella, 388

Parmacellidae, 157, 158 Placophora, 371, 385-388, 393-397, 400, 403-418
Partula, 2 Placuna, 24, 31

parva, Barnea, 130, 136, 143 ; plana, Scrobicularia, 15-21

Patella, 2, 315, 390 Planaxidae, 286, 287

Patellacea, 296, 310, 314, 353, 354, 358 planetica, Cardiomya, 51

Patellida, 391, 395 planispira, Saduniella, 217

Patellina, 310 planulata, Helicotoma, 324
paucidentata, Dorymenia, 384, 385 Platyacridae, 313, 335

Pecten, 23, 25, 26, 28, 29 Platyceras, 333

Pectinacea, 23-23 Platyceratacea, 311, 314, 330, 333
pectinata, Jouannetia, 136, 143 Platyceratidae, 333

Pectinibranchia, 359 platypoda, Nematomenia, 380
Pectinidae, 23, 26-28, 32, 42, 46 Pleuroceridae, 286

pectunculoides, Bathyarca, 69 Pleuromyidae, 50

pedicellatus, Lyrodus, 139, 144 pleuronectes, Amusium, 28

Pedum, 23, 26-31 Pleurotomaria, 357

Pelagiella, 331 Pleurotomariacea, 292, 310, 312, 314, 323, 324,
pellucida, Hubendickia, 218 331, 354

penelevis, Limopsis, 93 Pleurotomariidae, 292, 296, 298, 304, 310, 312,
Penicillus, 43 321, 331

penis, Brechites, 43 Pleurotomariina, 331

penita, Penitella, 136, 143 Pleurotomarioidea, 325

Penitella, 117, 130, 135, 136, 143, 144 plicaria, Terebra, 354, 365
pentangulatus, Euomphalus, 313 plicatula, Hastula, 364, 366

peregra, Lymnaea, 5-13 Plicatulacea, 23, 32

Perforatella, 151 Plicatulidae, 23

perieri, Limopsis, 83 pliocenicum, Terebra, 364, 365, 367, 368
Periploma, 53 poculifer, Teredo, 130, 133, 140, 144
Periplomatidae, 36, 39-42, 49, 50, 53-56 Pododesmus, 27

permagna, Neomenia, 381 Poiretia, 160, 161

Perna, 74 poirieri, Paraprososthenia, 217
Pernopectinidae, 27 Poleumitidae, 313

perroquini, Diplommatina, 204 polita, Hubendickia, 217, 218, 220

perroquini, Macropalaina, 204 Polygyracea, 157

428 MALACOLOGIA

Polygyridae, 150, 157

Polymesoda, 52

polypapillata, Spengelomenia, 382
Polyplacophora, 386-388

polythalamia, Kuphus, 130, 133, 137, 143
polyzonias, Sertularella, 382

Pomacea, 361

Pomatias, 170

Pomatiopsidae, 209-262
Pomatiopsinae, 209-262

Pomatiopsis, 209-262

Porites, 28

Poromya, 45, 47, 50, 51, 56
Poromyacea, 35, 36, 39, 44, 45, 48-50, 53-57
Poromyida, 391

Poromyidae, 36, 38, 44-47, 49-51, 54, 56
porosa, Heathia, 380

portoricensis, Teredo, 144

Potamididae, 283, 286, 287
praedatoria, Proneomenia, 384
praegnans, Pruvotina, 381

praestans, Xylophaga, 122, 136, 143
praetenue, Cochlodesma, 41

princesae, Teredora, 130, 133, 134, 144
prisca, Archaeomenia, 379, 380
procera, Spengelomenia, 382
Prochaetoderma, 373-377
Prochaetodermatidae, 376
Procrucibulum, 309

producta, Tomichia, 225, 230, 262
profunda, Dorymenia, 384

profunda, Xylophaga, 136

Progalerinae, 332

Progalerus, 309

Proneomenia, 379, 384
Propeamussiidae, 23, 26-28, 32
Propeamussium, 27, 28

proprietecta, Neomenia, 381

Prosobranchia, 177-289, 292, 354, 360, 363, 368

390, 391, 393-395
protecta, Forcepimenia, 382
Protobranchia, 391, 395
Protocalyptraea, 309
Pruvotina, 378, 381, 382, 395
Pseudomalaxis, 334
Pseudophoracea, 292, 311, 314, 330, 332, 333
Pseudophoridae, 333
Psilodens, 373, 376, 395

Psiloteredo, 116, 117, 123, 130, 133, 134, 137,

140, 144
Ptenoglossa, 391
Pteriacea, 23, 24, 26, 75
Pteriidae, 24
Pterioida, 24, 35, 53-55, 57
Pteriomorpha, 24
pulchella, Teredo, 116
Pulmonata, 5-13, 310
Punctinae, 157, 158
Punctum, 168
Pupillacea, 157
Pupillidae, 157, 158, 169
Pupillinae, 163
Pyramidulidae, 157, 158
Pyrazus, 282

quadra, Pholadidea, 130, 136
quadridens, Imeroherpia, 381
quadrizonata, Parapholas, 144
quillingi, Jouannetia, 136, 143
radians, Calyptraea, 214, 220
raduliferum, Prochaetoderma, 375, 376
ravni, Limopsis, 71

recisum, Chaetoderma, 375

rectum, Chaetoderma, 375

reedsi, Amphiscapha, 313

regularis, Strophomenia, 383
renschi, Teredo, 144

reticulare, Terebra, 364, 365, 367, 368
Retinella, 169

reynei, Neoteredo, 130, 133, 137, 143
Rhipidoglossa, 325

Rhipidoherpia, 379, 384
Rhopalomenia, 379, 382, 385
rhynchopharyngeata, Rhopalomenia, 382
Riftia, 292, 295, 307, 308

rikuzenica, Xylophaga, 136, 143
Rissoa, 392

Rissoacea, 354

Rissoidae, 285

rivicola, Lignopholas, 130, 136, 143
Robertsiella, 212

robustus, Scutopus, 373, 376, 377
rochi, Bankia, 144

rogersi, Hydrobia, 262

rogersi, Tomichia, 209-262
rolfbrandti, Jullienia, 217

rolfbrandti, Lacunopsis, 214

rosea, Genitoconia, 380

rostrata, Nettastomella, 130, 136, 143
rubiginosa, Zenobiella, 151

rubrum, Corallium, 380

ruizana, Limopsis, 81

Saccoglossa, 385

Saduniella, 211, 212, 214, 217
Salicornia, 231-233

salleana, Hastula, 367, 368

Sallya, 332, 333

sanctaemariae, Helixena, 151, 174, 175
Sandalomenia, 380

sansibarica, Limopsis, 81

saulii, Nausitora, 144

saxicola, Entodesma, 37

scalaris, Limopsis, 72

scandens, Strophomenia, 384
Scaphopoda, 387, 391, 393-397, 400
schizoradulata, Simrothiella, 378
Schizothaerus, 107, 108

schneideri, Nausitora, 144
Scissurella, 357

Scissurellidae, 296, 331

scotiana, Limopsis, 93

Scrobicularia, 15-21

Scutopoda, 372, 396

Scutopus, 372, 374-377
Seguenziacea, 325

Seguenziidae, 296, 311, 315
senegalensis, Psiloteredo, 130, 133, 144
senegalensis, Terebra, 364-366, 368
Sepia, 393

INDEX TO VOL. 21 429

Septemchitonida, 416

septemradiatus, Chlamys, 28

Septibranchia, 391, 395, 396

Septibranchoidea, 36, 50

Serpulorbis, 284

Serpulospira, 313, 315, 317

Sertularella, 382

sertulariicola, Rhopalomenia, 382

Sertulariidae, 382

setacea, Bankia, 130, 133, 144

Sialoherpia, 383

siamensis, Hubendickia, 218

siberutensis, Limopsis, 81

sierra, Eleutheromenia, 381, 385

Sigmurethra, 157, 158

Similis, Barnea, 144

simplex, Micromenia, 380

Simrothiella, 378

sinuosum, Guianadesma, 35, 53

Siphonodentaliida, 392

Siphonopoda, 372, 387, 390, 392-397, 400

Skeneidae, 296, 311

sluiteri, Proneomenia, 379

smithi, Diplothyra, 130, 136

smithi, Teredothyra, 144

soboles, Limopsis, 62, 69, 93

Solemyida, 391

Solenidae, 56

Solenogastres, 371, 377-379, 385, 393, 395-397,
400, 401, 403, 413, 414, 416

solidissima, Mactra, 101

somersi, Teredo, 144

sopita, Pruvotina 382, 385

soyoae, Limopsis, 90

spatha, Spathoteredo, 130, 133, 144

Spathoteredo, 117, 123, 130, 133, 134, 144

Spengelomenia, 382

spermathecata, Lituiherpia, 381

sphaerica, Lacunopsis, 214

Sphaeroma, 111

Sphincterochilinae, 150, 151, 153, 158, 174

spicata, Limopsis, 83

spinosa, Anamenia, 383

spinosa, Labidoherpia, 382

spinosa, Pachydrobia, 215

spinulosum, Craspedostoma, 335

spiralis, Hubendickia siamensis, 218

spiralis, Lophomenia, 382

Spisula, 95, 101

Spondylidae, 23, 26, 27, 32, 46

spondyloideum, Pedum, 27-29

Spondylus, 26, 27, 32

Sputoherpia, 383

Squamosum, Chaetoderma, 376

Stenzelia, 72

Sterrofustia, 381

stillerthrocytica, Proneomenia, 384

stimpsoni, Limopsis, 83

Stomatellidae, 310, 311, 333

strangei, Palaina, 205, 207

Straparollus, 313, 317

Streptaxidae, 173, 175

Striarcinae, 72

Striata, Hastula, 364-366

striata, Martesia, 112, 116-121, 130, 136, 138, 143

Striata, Myadora, 37, 39

Strioterebrum, 364, 365

Strobilopsinae, 157, 158

Strombidae, 263, 287

Strombus, 287

Strophomenia, 379, 380, 383-385

stylastericola, Dondersia, 380

Stylasteridae, 380

Stylommatophora, 149, 171, 173

subcinerea, Hastula, 364, 366, 367

subpersonatum, Isognomostoma, 150, 164

subtruncata, Barnea, 130, 136, 143

Subulinidae, 157, 158, 175

Succineacea, 157

Succineidae, 157, 158

suessi, Anisostoma, 335

sulcata, Hubendickia, 217, 218, 220

sulcata, Limopsis, 83

supplicata, Xvlophaga, 136, 143

surinamensis, Limopsis, 81

symbolicum, Campanile, 263-289

symmetrica, Holopea, 333

Syncyclonemidae, 27

Syngenoherpia, 384

Syntheciidae, 382

Tacheocampylaea, 151

tajimae, Limopsis, 81

takanoshimensis, Lyrodus, 133, 144

Talona, 117, 130, 135, 136, 143

talpoideus, Limifossor, 375, 376

tasmani, Limopsis, 83

Teiichispira, 330

Telescopium, 280-282

Tellinacea, 15-21, 46

tenella, Limopsis, 62, 63, 67, 74, 81, 82

tengulata, Nematomenia, 379, 380

tenisoni, Limopsis, 90

tenuiradiata, Limopsis, 90

teramachii, Xylophaga, 144

terceirana, Leptaxis, 175

Terebra, 364-368

Terebralia, 281, 282

Terebridae, 363-369

terebrinum, Terebra, 365

Teredina, 115, 116

Teredinidae, 111-148

Teredininae, 115-117, 124, 127, 138, 139, 143

Teredo, 111-148

Teredora, 116, 117, 123, 130, 133, 134, 135, 144

Teredothyra, 117, 123, 130, 133, 134, 137, 143,
144

Testacellacea, 157

Testacellidae, 157, 158

tetragona, Arca, 62

Thais, 12

Theba, 174

thermydron, Bythograea, 307

Thiaridae, 287

thoracites, Bactronophorus, 130, 133, 137, 143

Thracia, 39-42, 49, 54, 55

Thraciacea, 35, 36, 39-42, 44, 49, 50, 53-57

Thraciidae, 36, 39-42, 49, 53-57

Tibia, 287

430 MALACOLOGIA

Tivela, 98, 103, 107

Tomichia, 209-262

tomlini, Xylophaga, 144

tornata, Poromya, 47

torresi, Limopsis, 90

totteni, Hydrobia, 218, 219

trapeziformis, Neomenia, 381

triangularis, Anamenia, 383

triangularis, Teredo, 144

tricarinata, Dorymenia, 384

tricarinata, Rhopalomenia, 382

Trichiinae, 150

Tricula, 209-262

Triculinae, 209-262

Triculini, 209-262

Triforidae, 368

Triforis, 368

triglandulata, Metamenia, 382

Trigoniacea, 35, 53

Trigoniidae, 287

Trigonochlamydidae, 157, 158

Trinacriinae, 72

trisialota, Birasoherpia, 383

tristis, Hydrobia, 225

tristis, Tomichia, 209-262

Trochacea, 291-336, 353-355, 361

Trochidae, 296, 311, 317, 335, 359

Trochina, 310, 311, 314, 325, 333

Trochita, 332

Trochoidea, 151

Trochoidea, 325

Trochonematacea, 334

tropicus, Bulinus, 234

truncata, Barnea, 136, 143

truncata, Laternula, 42

Truncatella, 225

truncatum, Cerithium, 282

Tryblidiida, 371, 388-390, 393, 395-397, 400, 413-
415

tuberculata, Hubendickia, 217

tubifera, Pholadidea, 130, 136, 143

tubulata, Xylophaga, 136, 143

Turbellaria, 395

Turbinaria, 29

Turbinidae, 296, 311, 316, 317, 334

Turbinilopsis, 316

turnerae, Penitella, 144

turnerae, Xylophaga, 130, 136, 143

turricula, Discula, 151, 175

turricula, Hystricella, 151

Turritella, 319, 321, 322, 332

Turritellidae, 285-287, 291, 321, 322

Tyrodiscus, 169

Umbonium, 311, 324, 333, 359

uniperata, Pruvotina, 381

Uperotus, 117, 123, 130, 133, 134, 135, 143, 144

usarpi, Dorymenia, 379, 384

Utralvoherpia, 383

vaginata, Limopsis, 62, 63, 67, 80, 82

Valloniidae, 157, 158

Valloniinae, 157, 158

Valvata, 285

Valvatacea, 360, 361

vampyrella, Drepanomenia, 383

varia, Chlamys, 28, 29

variabilis, Pachydrobia, 215, 218
Velepalaina, 180

Velutina, 284

Vema, 389, 390

Veneroida, 35, 53-55, 57

ventricosa, Tomichia, 209-262
ventricosa, Truncatella, 225
ventrolineatus, Scutopus, 372, 374-377
Vermetidae, 285-287

Vermetus, 284

verrucosa, Epimenia, 384, 385, 401
Verticordiacea, 35, 50, 51, 54-57, 391
Verticordiidae, 36, 39, 44, 45, 47, 49-51, 54-56
Vertiginidae, 157, 158
Vetigastropoda, 325

vetusta, Leptaxis, 175

vetustum, Platyceras, 333
villosiuscula, Thracia, 39-41

virginica, Crassostrea, 99, 108
Vitreinae, 157, 158

Vitrinidae, 157, 158, 169

vittatus, Donax, 101, 102, 105, 108
Viviparacea, 360, 361

Viviparus, 323

vixinsignis, Epimenia, 384

vixornata, Limopsis, 65, 70, 72, 91
Volutacea, 368

Volutidae, 285

Vulsella, 74

washingtona, Xylophaga, 122, 130, 136, 143
weberi, Dorymenia, 384

Weeksia, 313, 314, 316, 320
Weeksiidae, 312, 314, 320

whitneyi, Omphalotrochus, 313

whoi, Xylophaga, 136

Wireniidae, 401

wolfi, Xylophaga, 136, 143
woodwardi, Limopsis, 90
Xenophoridae, 317

Xeropicta, 150

Xerosecta, 150

Xerotricha, 174

xylophaga, 111-148

Xylophagainae, 111-148
Xylophaginae, 115

Xylopholas, 115, 117, 124, 130, 135, 136, 143
Xylophoma, 115

Xyloredo, 115-117, 124, 130-137, 143
yoshimurai, Aspidopholas, 144
Zachsia, 117, 130, 133, 139, 144
Zebrina, 160

zenkewitschi, Zachsia, 130, 133, 139, 144
Zenobiella, 151, 173

zeteki, Bankia, 144

zevinae, Neolepas, 321

zilchi, Pachydrobia, 215

Zirfaea, 117, 130, 135, 136, 143
Zoantharia, 383

zonalis, Limopsis, 81

Zonitinae, 157, 158, 160, 162
Zonitacea, 157

Zonitidae, 157-159, 169
zwellendamensis, Paludina, 225
zwellendamensis, Tomichia, 209-262

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INSTRUCTIONS FOR AUTHORS

MALACOLOGIA publishes original studies
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1981

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VOL. 21, No. 1-2 MALACOLOGIA 1981

CONTENTS
SECOND INTERNATIONAL SYMPOSIUM ON EVOLUTION
AND ADAPTIVE RADIATION OF MOLLUSCA
SPONSORED BY
UNITAS MALACOLOGICA
SEVENTH INTERNATIONAL MALACOLOGICAL CONGRESS
PERPIGNAN, FRANCE. 31 August-7 September 1980

G. M. DAVIS
Introduction to. Symposium. „u... 2.0.8 i oo 24 Pr 1

P. CALOW

Adaptational aspects of growth and reproduction in Lymnaea

peregra (Gastropoda: Pulmonata) from exposed and shel-

tered) aquatic Mabitats = en... LA SM RE SR un + 25 ha oo 5
Е. В. TRUEMAN and H. В. AKBERALI

Responses of an estuarine bivalve, Scrobicularia plana (Tellinacea)

PE Mani CS D SE RENE NO d'EPS и ОА RA 15
С. М. УОМСЕ

On adaptive radiation in the Pectinacea with a description of Hemi-

neelen o et un ARRET a N PR TERRE 23
B. MORTON

The: Anomalodesmata 22 coa aa e а tears s 35
P. G. OLIVER

The functional morphology and evolution of Recent Limopsidae

(Bivalvia, Arcoidea) Dic. и, al das piel 0 SN ee A 61
W. NARCHI

Aspects of the adaptive morphology of Mesodesma mactroides

(Bivalvia Mesodesmatidae) 242240044420 24 a2 2 00 AN 95
K. E. HOAGLAND and R. D. TURNER

Evolution and adaptive radiation of shipworms (Bivalvia, Teredinidae) ....... 111
A. J. CAIN

Variation in shell shape and size of helicid snails in relation to

other pulmonates in faunas of the Palaearctic region ...................... 149
S. TILLIER

Clines, convergence and character displacement in New Caledonian

diplommatinids (land: prosobranchs) <7 ¿cocoa ar ASE 177
G. M. DAVIS

Different modes of evolution and adaptive radiation in the

Pomatiopsidae (Prosobranchia: Mesogastropoda) ......................... 209

R. S. HOUBRICK
Anatomy, biology and systematics of Campanile symbolicum with
reference to adaptive radiation of the Cerithiacea (Gastropoda:

Prasabranchla). ls dos chai he TRE RAS oe de ASE RSR ee EEE 263
J. H. MCLEAN

The Galapagos rift limpet Neomphalus: relevance to under-

standing the evolution of a major Paleozoic-Mesozoic radiation ............ 291
V. FRETTER, A. GRAHAM and J. H. McLEAN

The anatomy of the Galapagos rift limpet, Neomphalus fretterae ........... 337
Р. BOUCHET

Evolution of larval development in eastern Atlantic Terebridae

(Gastropoda), .'Neagene to Recente Us ее 363
L. v. SALVINI-PLAWEN

The molluscan digestive system in evolution .............................. 371
W. HAAS

Evolution of calcareous hardparts in primitive molluscs .................... 403

INDEX TO VOLUME 21, No. 1-2

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