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VOL. 3 1965-1966
MALACOLOGIA
International Journal of Malacology
Revista Internacional de Malacologia
Journal International de Malacologie
Международный Журнал Малакологии
Internationale Malakologische Zeitschrift
MUS. COMP. ZOOL.
LIBRARY
JUN 21 1966
HAR Va
UNIVERSITY
DATES OF PUBLICATION
At least 50 copies of MALACOLOGIA were mailed to subscribers (including a free
copy to the Library of Congress, Washington, D. C.) on the following dates:
Vol. II, No. 1 August 31, 1965
Vol. Ш, No. 2 December 9, 1965
Vol. HE No.3 May 31, 1966
iv
MALACOLOGIA, VOL. 3
CONTENTS
. J. BOSS
Symbiotie eryeinaeean Divalves.. . .... еее...
. R. CLARKE
“Growth rings” in the beaks of the squid Moroteuthis ingens
(Oeconsidacs Onychoteuthidae) =. iy. ar... 4 4h Joue, eb e
. C. DAZO
The morphology and natural history of Pleurocera acuta and
Goniobasis livescens (Gastropoda: Cerithiacea: Pleuroceridae)
. H. FRANK and A. Н. MEYLING
A contribution to the conchometry of Biomphalaria pfeifferi
IBasemmatophbora:, Planorbidae) o. be ke ee Zac...
. T. GHISELIN
Reproductive function and the phylogeny
Портосе PaAStrOpods 060 «eae a nt dora cette el,
. O. GREGG and D. W. TAYLOR
Fontelicella (Prosobranchia: Hydrobiidae), a new genus of west
AMERICAN. TreEShwateriSnarlis: не Soc ene bse Reese nies
. N. GRUSOV
The endoparasitic mollusk Asterophila japonica
Randall and Heath (Prosobranchia: Melanellidae)
and its relation to the parasitic gastropods ..............
. LAURSEN
Dhereenus-Myain'the-Aretie region... 2... 20 0 0 LU a aw hee
. L. McALESTER
Evolutionary and systematic implications of a transitional
Ordeyieianzlucinoidäpivalvery. Le as ee eee ee
. McCLARY
Statocyst function in Pomacea paludosa
(Mesogastropodas-Ampullariidae) 71.12. IH 2 ee:
. MARCUS
Some Opisthobranchia from Micronesia... 2.6. еее.
. MARCUS and J. B. BURCH
Marine euthyneuran Gastropoda from Eniwetok Atoll,
WEST aci cle dence т.
MALACOLOGIA, VOL. 3
К. N. NESIS
Ecology of Cyrtodaria siliqua and history of the genus
Cyrtodaria (Bivalvia: Hiatellidaeht ........ 2... ao ae ee 197
C. M. PATTERSON and J. B. BURCH
The chromosome cycle in the land snail Catinella vermeta
(Stylommatophora: (Succineidae) aici te una cha Naar Fame oie 309
H. VAN DER SCHALIE and G. M. DAVIS
Growth and stunting in Oncomelania (Gastropoda: Hydrobiidae)..... 81
S. K. WU
Comparative functional studies of the digestive system of
the muricid gastropods Drupa ricina and Morula granulata........ 211
vi
Tom 3 МАЛАКОЛЕНИЕ Май 1966
ОГЛАВЛЕНИЕ
Страница,
К. КЕННЕТ
Симбиотические двустоврчатые надсемейства,
Еяус ac ea . . . . . . . . . . . . . . . . . . . . . o . . 183
MATES КЛАРЕЗ
"Кольца роста" на клюве кальмара Moroteuthis ingens
(Oegopsida: Onychoteuthidae). «5 = «5 ее + + + + + te о we COT
Б. К. ДАЗО
Морфология и история жизни Pleurocera acuta и Goniobasis
livescens (Gastropoda: Cerithiacea: Pleuroceridae). ........ 1
Г. X. ФРАНК И A. X. МЕЙЛИНТ
Конхометрия пресноводной улитки Biomphalaria pfeifferi
(Basemmalophprar Planorbidae) 2 y lie a nm... a 5819
ШТ. гИЗЛИЕ
Репродуктивные Функции и Филогения заднежаберных
ВЕН О оков «ee Gu. a Da at an QUE ae аъ ae
В. 0. ГРЭГГ ИД. В. ТЭЙЛОР
Fontelicella (Prosobranchia: Hydrobiidae),
новый pol. западно-американских пресноводных улиток. . . „103
ВЕ. ГРУЗОВ
Зндопаразитический моллюск Asterophila japonica
Randall et Heath (Prosobranchia: Melanellidae)
и его связь с паразитическими брюхоногими +. +. + +. + + + .111
Д. ЛАРСОН
Примета А i Mlle, По Le ее сб в 9999
А. Ли. МкАЛИСТЕР
Эволюционные и систематические проблемы
промежуточных люциноидных двустворчатых +. 2 + + + + + + 2433
А. МаккЛЕЙРИ
Функционирование статоцистов у пресноводной
улитки Ротасеа paludosa (Mesogastropoda: Ampullariidae) . . . . .419
Э. МАРКУС
Некоторые заднежаберные моллюски из мкронезии +. +. + + + .263
Ш
Э иМАРКУ СТИ. Б.'БЕБУ
Морские брюхоногие моллюски подкласса Euthyneura
из атолла зниветок западной части великого океана . +. . .235
vii
МАЛАКОЛЕНИЕ
К. H. НЗЗИС
Экология Cyrtodaria siliqua и история жизни рода
Cyriodaria (BivalvianHiatelidae). 2. 1. le masa нее м
№
С. Mo ПАТТЕРСОНИИ Me. Bs БЕРЧ
Хромосомные циклы у наземиой улитки Catinella vermeta
(Stylommatophora: Succeineidae). „ее 2.0 © 0. in Oe
Г. ВАН ДЕР ШАЛЭ И Г. М. ДЭЙВИС
Рост и его замедление у Oncomelania
(Gastropoda Нуакорнаае) зо о с о RC
Mo о ВА
Сравнительное исследование пищеварительного
процесса у брюхоногих Drupa vicina и Morula granulata . . . . „211
viii
MALACOLOGIA, VOL. 3
NEW NAMES
GASTROPODA
Fontelicella, Gregg & Taylor, 1965, 103
californiensis, (Fontelicella), Gregg & Taylor, 1965, 109
Natricola, Gregg & Taylor, 1965, 108
Microamnicola, Gregg & Taylor, 1965, 109
musetta, (Haminoea), Marcus € Burch, 1965, 239
linda, (Haminoea), Marcus € Burch, 1965, 241
briqua, (Chromodoris), Marcus € Burch, 1965, 245
mietta, (Herviella), Marcus € Burch, 1965, 252
evelinae, (Onchidella), Marcus € Burch, 1965, 253
illus, (Stiliger, Ercolania), Marcus, 1965, 267
bayeri, (Elysia), Marcus, 1965, 270
тата, (Elysia), Marcus, 1965, 270
cuis, (Hypselodoris), Marcus, 1965, 272
lora, (Discodoris), Marcus, 1965, 273
ylva, (Discodoris), Marcus, 1965, 275
lonca, (Catriona), Marcus, 1965, 279
urquisa, (Catriona), Marcus, 1965, 279
rehderi, (Noumeaella), Marcus, 1965, 282
evelinae, (Muessa), Marcus, 1965, 283
Muessa, Marcus, 1965, 282
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VOL. 3 NO. 1 AUGUST 1965
MALACOLOGIA
1
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MUS. COMP ZOO!
LIBRARY
SEP 16 1905
HARVARD
ternational Journal of Malacology
Revista Internacional de Malacologia
Journal International de Malacologie
Международный Журнал Малакологии
Internationale Malakologische Zeitschrift
MALACOLOGIA
ANNE GISMANN, General Editor
19, Road 12 +
Maadi, Egypt
UA. Re
J. B. BURCH, Managing Editor
Museum of Zoology
The University of Michigan
Ann Arbor, Mich. 48104, U.S.A.
EDITORIAL BOARD
SCHRIFTLEITUNGSRAT
P. O. AGÓCSY
Magyar Nemzeti Múzeum
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Budapest, VIII., Hungary
C. R. BOETTGER
Technische Hochschule
Pockelsstrasse 10a
Braunschweig, Germany
A. H. CLARKE, JR.
National Museum of Canada
Ottawa, Ontario
Canada
C. J. DUNCAN
Department of Zoology
University of Durham
South Rd., Durham, England
E. FISCHER-PIETTE
Mus. Nat. d’Hist. Natur.
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Paris V®, France
A. FRANC
Faculté des Sciences
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Paris V©, France
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National Science Museum
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Tokyo, Japan
A. D. HARRISON
University College of
Rhodesia & Nyasaland
Salisbury, Rhodesia
K. HATAI
Inst. Geology & Paleontology
Tohoku University
Sendai, Japan
РЕДАКЦИОННАЯ КОЛЛЕГИЯ
N. А. HOLME
Marine Biological Assoc. U.K.
The Laboratory, Citadel Hill
Plymouth, Devon, England
G. P. KANAKOFF
Los Angeles,County Museum
900 Exposition Boulevard
Los Angeles, Calif., 90007, U.S.A..
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Department of Geology
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Bernice P. Bishop Museum
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U.S. A.
H. LEMCHE
Universitetets Zool. Museum
Universitetsparken 15
Copenhagen ®, Denmark
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Faculty of Medicine
Haile Sellassie 1 University
° Addis Ababa, Ethiopia
N. MACAROVICI
Laboratoire de Géologie
Université “Al. I. Cuza”
Iasi, Romania
D. F. McMICHAEL
The Australian Museum
College Street
Sidney, Australia
J. E. MORTON
Department of Zoology
The University of Auckland
Auckland, New Zealand
У. К. OCKELMANN
Marine Biological Laboratory
Grönnehave, Helsingór
Denmark
J. M. HUBER, Associate Editor
Museum of Zoology
The University of Michigan
Ann Arbor, Mich. 48104, U.S.A.
CONSEJO EDITORIAL
CONSEIL DE REDACTION
W. L. PARAENSE
Centro Nacional de Pesquisas
Malacológicas, C. P. 2113
Belo Horizonte, Brazil
J. J. PARODIZ
Carnegie Museum
Pittsburg, Penn., 15213,
К.А,
В. О. РОВСНОМ
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Technology
London, S. W. 3, England
S. G. SEGERSTRÄLE
Zool. Mus. Helsinki University
P. -Rautatiekatu 13
Helsinki, Finland
F. STARMÜHLNER
Zool. Inst. der Universität Wien
Wien 1, Luegerring 1
Austria
J. STUARDO
Instituto Central de Biologia
Universidad de Concepcion
Cas. 301, Concepcion, Chile
W.S.S. VAN BENTHEM JUTTING
Noordweg 10 :
Domburg
The Netherlands
J. A. VAN EEDEN
Inst. for Zoological Research
Potchefstroom Univ. for C.H.E.
Potchefstroom, South Africa
C. M. YONGE
Department of Zoology
The University
Glasgow, Scotland
A. ZILCH
Senckenberg-Anlage 25
6 Frankfurt am Main 1
Germany
LS к nn
MALACOLOGIA was established with the aid of a grant (NSF-G24250) from the National Science Foundation,
Washington, D. C,, U.S. A.
MALACOLOGIA wurde unter Beihilfe einer Unterstützung (NSF-G24250) der National Science Foundation,
Washington, D. C., U. S. A., gegründet.
MALACOLOGIA fut établi avec l’aide d'une subvention (NSF-G24250) de la National Science Foundation,
Washington, D. C., U.S. A.
MALACOLOGIA fue establecida con la ayuda de una subvencion (NSF-G24250) de la National Science
Foundation, Washington, О. C., Ц. 5. A.
Журнал МАЛАКОЛОГИЯ был подготовлен к изданию при
дарственного научного общества в Вашингтоне, США.
помощи субсидии (NSF - 624250) or Tocy-
MALACOLOGIA, 3(1):1-80, 1965
THE MORPHOLOGY AND NATURAL HISTORY OF
PLEUROCERA ACUTA AND GONJOBASIS LIVESCENS WUS COMP. 7001
(GASTROPODA: CERITHIACEA: PLEUROCERIDAE)!,2 LIBRARY
Bonifacio Capili Dazo3 SFP 16 1909
ABSTRACT HARVARD
DNIVERSI]
Relatively little is known about the Pleuroceridae, a family of freshwater
operculate snails common in North America, which comprises, or is related
to, medically important melaniid snails in the Far East. Their taxonomy,
largely based on shell characteristics, is generally in need of revision. A com-
parative study was made of the morphology and biology of 2 species classified
in 2 different genera: Pleurocera acuta Rafinesque and Goniobasis livescens
(Menke), originating from 4 stations near Ann Arbor, Michigan, and from
additional localities in Michigan and Ohio, U. S. A.
The shells and opercula of these 2 species differ: however, the similarities
not only of their internal anatomy but also in the general pattern of their life
history are so striking, that their position in 2 separate genera is open to
question.
Differences in the shell, though quite marked, are not always present, and
were hardly discernible in some intermediate specimens. P. acuta is about
twice as large. Although the general form and pigmentation of the body are
quite similar, P. acuta has a more elongated snout and head-trunk region, and
longer and more tapering tentacles. It has a smaller and more elongate foot
which may be an adaptation to its bottom dwelling and burrowing habit, while
G.livescens has a rounder and larger foot in relation to the head region, which
may be associated with its crawling habit. The mantle and sense organs, the
general organization of the nervous system, the morphology of the respiratory,
excretory, digestive, circulatory and the muscular systems of both species
are quite similar; they differ only in size. In the Pleurocerinae the males
have no penis. Females have a deep reproductive pit in the neck between the
right tentacle and the base of the foot, and a shallow reproductive groove
leading to this pit. Otherwise the general pattern in the reproductive system
conforms with that of other prosobranchs. The sexes are separate. In both
species the reproductive organs of each sex were almost identical and occu-
pied the same position. Spermatozoa were of 2 types: the typical (eupyrene)
and the atypical (apyrene) form. The former are transferred to the female in
spermatophores.
Ecologically, the North American pleurocerids require clean water. Except
for Goniobasis they all prefer relatively large habitats. They usually live in
sandy or muddy areas in the sheltered portions of streams. Goniobasis lives-
cens is found in almost any clean and permanent type of fresh-water environ-
ment (springs, swift flowing streams, inland lakes); this species is usually
LA dapted from a dissertation submitted in partial fulfillment of the requirements for the degree
of Doctor of Philosophy at the University of Michigan.
2This investigation was supported (in part) by a research grant, 5 T1 Al 41-05 (2E-41), from
the National Institute of Allergy and Infectious Diseases, U. S. Public Health Service.
3Present Address: World Health Organization, Regional Office for the Eastern Mediterranean,
Alexandria, Egypt, U. A. R.
(1)
B. C. DAZO
found crawling on rocks and stones.
Both the laboratory and field observations indicated that mating takes place
during the fall. When the temperature falls below 5°C the animals hibernate.
They resume activity and begin to lay eggs in spring. The sand-covered eggs
of P. acuta are laid in batches of varying sizes and shapes; the number of eggs
per mass varies from 1-19. G. livescens lays eggs singly, sometimes 2-3in
a row and several centimeters apart; these are usually covered with a thin
layer of soil. P. acuta has a greater egg output than С. livescens (15 eggs
snail/day as against 4) but has a shorter period of egg-laying (April to June
against April to mid-August). In both species embryonic development lasts
about 2 weeks.
Growth was most pronounced during the first year (from 0.3 to 10 mm in
P. acuta;, 0.3 to 3.8 mm in С. iivescens). When the laboratory-bred snails
attained sexual maturity, at 2 years, they were 16.7 and 7 mm long, respec-
tively, after which time no appreciable growth occurred. Environmental snails
were larger. The normal life span is 3 years but may perhaps extend to 4
years. In P. acuta the sex ratio was about 2:1 in favor of the females; in G.
livescens about 5:1. As other prosobranchs, both species feed on red and
green algae, desmids, and diatoms. Larval trematodes belonging mainly to
the families Azygiidae, Allocreadiidae and Aspidogastridae often heavily para-
sitized the liver, gonad, alimentary tract and other organs.
CONTENTS Page
Page Reproductive System . . 2.200 35
Male Reproductive System ... . 36
INFRODUC TION es sso ule ae are 3 Female Reproductive System . . 38
SYSTEMATIC POSITION AND Muscular System... ооо 40
HISTORICAL REVIEW :2%:..#.1. 40 3 ECOLOGICAL STUDIES... + 782 41
DISTRIBUTION ............... 9 Description of Habitats... se. 41
Geologic Distribution. ......... 9 те — i
Geographic Distribution........ 10 Some athe leo eee
METHODS AND TECHNIQUES.... 11 Michigan .. ...-. VER 43
Sampling Methods ......... Ses Collecting site in Ohio ....... 44
Limnological Methods ......... 12 Vegetation .. „u. 2... o 46
Maintenance in the Laboratory ... 13 Limnological data. ..... . 0e 46
Preparation of Materials for Influence of Environmental
Anatomical Studies ......... 14 Factors.on Shell... ha ee 51
Histological Methods. ......... 16 LIFE HISTORY............... 55
MORPHOLOGICAL STUDIES ...... 16 Mating Habits? i 2). . EEE 55
Shell and’ @perculund . "2... 22... 16 The Egg and Egg-laying
PEUR REPIONE AN и. 19 Activities 2.5.0... ete eee 56
senserOrgans it ee, 21 Time of Development in the Egg
NEFVOUS SYSTEME 0 elote en. cu 21 and gross Embryology....... 60
Digestive System? 1. codi do 26 Growth. ae CO 60
Alimentary iract 3/24 LL 28 Sexual Maturity and Longevity ... 61
Gtherorsansie.s tin ere 30 Sex: Ratio Hi CA Ce 63
Vascular Systems. 02905420 4 32 Diurnal and Seasonal
Excretory System. 4.2: . „u... 34 Activities. oo Sica eee 63
Respiratory System"... ......,. 35 Food and Feeding Habits....... 64
PLEUROCERA AND GONIOBASIS
Contents (cont.)
Page
Parasites and Predators ....... 66
DISCUSSION OF PLEUROCERID
RS ES e as er, 71
ACKNOWLEDGEMENTS ......... 13
Pires CURE, CITED ео. 74
INTRODUCTION
The melaniid snails of the family
Pleuroceridae are common and wide-
spread on the North American conti-
nent and are the dominant group of
fresh-water gastropods in the south-
eastern United States. Nevertheless,
little attention has been given to the
biology of this common prosobranch
family. Most of the existing literature
pertains to shell descriptions and shell
variation and only a few papers deal
with aspects of their morphology and
natural history.
There are several factors which con-
tribute to the neglect this family has
suffered: (1) Their greatest abundance
and the great majority of species occur
in the southeastern United States, which
has only recently developed research
facilities; (2) the great individual and
intrapopulation variation in the various
Species and the large number of names
superficially applied to this variation
has resulted in a taxonomic and nomen-
clatural confusion which is discouraging
to workers interested in working with
the group; and (3) there has been a
general failure to culture pleurocerid
snails successfully in the laboratory.
The purpose of this investigation was
to study aspects of the biology of
Pleurocera acuta Rafinesque and Gonio-
basis livescens (Menke). These 2 species
were selected because: (1) they are
common and readily available in the
Surroundings of Ann Arbor, Michigan;
(2) little is known of their biology;
(3) they are important in that they serve
as intermediate hosts for trematode
parasites of fresh-water fish and are
of interest to parasitologists in that
they harbor various other larval flukes;
and (4) they are related to medically
important melaniids in the Orient4 Also
it is hoped that the present work may
serve to lay a foundation for further
morphology and life history studies on
other members of the family and help
formulate a new evaluation and a more
meaningful revision of the systematics
of the Pleuroceridae.
SYSTEMATIC POSITION
AND HISTORICAL REVIEW
The Pleuroceridae belong to the sub-
class Prosobranchia which are usually
bisexual, operculate snails having the
gills in front of the heart and crossed
visceral nerve commissures producing
an 8-shaped loop. This family belongs
to the order Mesogastropoda Thiele,
which almost corresponds to the
Pectinibranchia of earlier authors or to
the Ctenobranchia excluding the Steno-
glossa, i.e. to the Taenioglossa. The
“taenioglossid” radula has 7 teeth, 3
on each side of the median tooth.
The systematic position of Pleurocera
acuta and Goniobasis livescens, slightly
modified from Thiele (1929), is as
follows:
Phylum Mollusca
Class Gastropoda Cuvier, 1797
Subclass Prosobranchia Milne-Ed-
wards, 1848 (Streptoneura
Spengel, 1881)
Order Mesogastropoda Thiele,
1925
Superfamily Cerithiacea Fleming, 1882
4Semisulcospira libertina end Thiara
(Tarebia) granifera, which act as the first
intermediate hosts of Paragonimus wester-
mani, the human lung fluke, and Melanoides
tuberculatus, which carries Clonorchis
sinensis, the oriental human liver fluke.
B. C. DAZO
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FIG. 1.
The distribution of Pleurocera acuta in North America.
PLEUROCERA AND GONIOBASIS
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VLOS3NNIN
FIG. 2. The distribution of Goniobasis livescens in North America.
6 B. C. DAZO
FIG. 3. The distribution of Goniobasis livescens in Michigan (From Goodrich, 1945).
PLEUROCERA AND GONIOBASIS 1!
FIG. 4. The distribution of Pleurocera acuta in Michigan.
8 B. C. DAZO
Family Pleuroceridae® Fischer,
1885
Subfamily Pleurocerinae Morrison,
19546
Genus Pleurocera Rafinesque,
1818
Species Pleurocera acuta™ Raf-
inesque, 1831
Genus Goniobasis Lea, 1862
Species Goniobasis livescens
(Menke), 1830
Morrison (1952, 1954) in an evalua-
tion of phylogenetic relationships of old
and new world melanians, based on the
morphology of the reproductive system
and on biological considerations, sug-
gested an arrangement in which all
freshwater melaniids were grouped in
3 families, each of which is directly
related to 3 marine families, as follows:
1) Melanopsidae-Modulidae; 2) Pleuro-
ceridae-Cerithiidae; and 3) Thiaridae-
Planaxidae. The first 2 groups are
SThe earlier family name Strepomatidae
Haldeman, 1863, must be rejected because
it is not basedon anavailable generic name.
A proposal for validation and inclusion in
the Official List of both the family Pleuro-
ceridae and the genus Pleurocera as its
type is now under the consideration of the
International Commission of Zoological
Nomenclature (Melville, 1960).
6Thiele (1929) listed Pleurocerinae as a
subfamily of Melaniidae.
ТВу longstanding usage the species acuta has
been treated as the type species of the
genus Pleurocera, whereas, by strict
application of the present rules of nomen-
clature, the type species ought to be “P.”
verrucosa. However, formal acceptance of
verrucosa would entail confusing transfers
of names; the snails now placed under
Lithasia Haldeman, 1963, would become
Pleurocera, while another name would have
to be resurrected for those now commonly
called Pleurocera. To avoid widespread
confusion, a request for the validation of P.
acuta as the type has been placed before the
I.C.Z.N. (Melville, 1960).
dioecious, while no males are present
in the third group, in which the females
reproduce parthenogenetically. The
families all belong in the superfamily
Cerithiacea. Rosewater (1960a) con-
siders the above proposals interesting
but not yet conclusive and believes that
some of the various relationships on
which it is based need to be further
investigated and evaluated before final
acceptance.
According to Morrison the charac-
teristics of the typical subfamily Pleuro-
cerinae, to which the North American
pleurocerids probably all belong, are:
the females, all oviparous, unfailingly
have an egg-laying sinus on the right
side of the foot; the males have no
intromittent organ.
Morrison, rejecting the name Pleuro-
cera. for the forms grouped under it by
Bryant Walker (1918), selected for them
the name Oxytrema Rafinesque, 1819,
and further combined under this genus,
on the basis of egg-laying characters,
most species of Goniobasis. He also
revived the genus Mudalia Haldeman,
1840 and, placed Goniobasis livescens
(Menke) under it.
The writer feels that the evidence
for this combination and the concomitant
transfers is as yet insufficient and
prefers to maintain the traditional
nomenclature until such a time when
more extensive study of the group con-
cerned will provide a broader basis
for revision.
For further details on the subject
the reader is referred to the section
“Discussion of Pleurocerid Systematics”
(p 71). In the following, a brief his-
torical review only is given of the early
literature pertaining to Pleuroceridae
to provide a background. The earliest
known pleurocerid records were those
by Lister (1770) and Gmelin (1791)
on Buccinum (-Goniobasis) virginicum.
In the early days all the pleurocerid
groups were assigned to the genus
Melania Lamarck (1792), which also
included all operculate fresh-water
gastropods other than those belonging
AAA AA A
PLEUROCERA AND GONIOBASIS 9
to the Viviparidae and Pilidae, from
all parts of the world. In due time
the heterogeneous condition within
the genus Melania was recognized and
various authors provided some relief
by splitting the group and introducing
new genera. In the following are listed
some of the most notable authors of
generic names for the pleuroceridgroup
of North America and their corres-
ponding contributions. C. S. Rafinesque,
in 1818, established the genus Pleuro-
cera, naming 6 species without giving
any descriptions; in 1819 he defined
Pleurocera and created the genus Oxy-
trema. The following year he described
the first recognizable species, Pleuro-
cera verrucosa (-Angitrema verrucosa)
and at the same time he also described
a species from Lake Erie, P. acuta.
Rafinesque’s failure to designate a type
for the genus Pleurocera has caused
contention, not only among his contem-
poraries, but also among many of his
successors (Walker, 1917) and the ques-
tion as to which species will ultimately
be accepted as the type species is not
yet settled. In 1819 he also named
the genus Leptoxis. According to
Morrison (1945) Leptoxis is the earlier
and valid name for the genus that Thomas
Say named Anculosa in 1821. Isaac
Lea? later proposed the 3 genera: Jo,
in 1831, Goniobasis, in 1862 and Eury-
caelon, in 1864; Shuttleworth, in 1845,
described the genus Gyrotoma; Halde-
man, in 1840, named the genera Muda-
lia, and Lithasia; Nitocris was named
by H. and A. Adams in 1854. Pilsbry,
in 1910, added the genus Lithasiopsis”.
H. and A. Adams (1854) established
Elimia as a subgenus of Pleurocera
8Lea also introduced Trypanostoma (a syno-
nym of Pleurocera) and Strephobasis as one
of its sections, but these are not in use to-
day.
2The position of this genus is dubious. I
share Goodrich’s (1942) opinion that Lithasi-
opsis probably is related to Pachy-
chilus.
and placed in it 16 species including
G. livescens; but among these were at
least 4 with obviously different kinship
(Goodrich, 1945). In 1896, Pilsbry
tried to revive Elimia, raising it to
generic rank, to take the place of
Goniobasis. Later, he decided that
Goniobasis should be restored as a
genus on the grounds that Elimia was
a composite group (Walker, 1918). The
earlier synonyms for the genus Pleuro-
cera are given in Tryon’s (1873) manual
on the Strepomatidae, p 49, while those
for the genus Goniobasis are listed on
p 138.
Among authors that have made valu-
able contributions to pleurocerid syste-
matics are: Hannibal, Conrad, Anthony,
DeKay, Hinds, Gould, Tryon, Menke, C.C.
Adams, Goodrich, and others. Their
contributions are too numerous to be
discussed here; however, Adams’ study
on Jo is listed in the references.
More detailed data on the literature
regarding the 2 species under consid-
eration, Pleurocera acuta and Goniobasis
livescens, and their close relatives, will
be given in the appropriate sections.
Unfortunately these records deal mostly
with descriptions of the shell and with
ecology, while information on the ana-
tomy and life history of these snails
is scarce. Most important among these
are Magruder’s (1935b) studies on the
anatomy of Pleurocera canaliculatum
undulatum which furnished a valuable
basis for the present study and will
be extensively quoted below. Worthy
of note are also the studies of Rose-
water (1959a, 1961) on P. canaliculata,
those of the cytologist Woodard (1934,
1935, 1940) on the reproductive system
and spermic dimorphism of Goniobasis
laqueata and Jewell’s (1920) observa-
tions on the reproduction of Goniobasis
livescens correcta.
DISTRIBUTION
Geologic Distribution.
Records exist for pleurocerids in
10 B. C. DAZO
strata ranging from the Cretaceous to
the Pliocene epoch. Although Weatherby
(1876) suggested that they appeared as
early as the Carboniferous age of the
Paleozoic era, or that immediately suc-
ceeding it, this has never been cör-
roborated. White (1882), Walker (1900),
and Adams (1915) were of the opinion
that the earliest fossil Pleuroceridae
are from the late Mesozoic Laramie
formation, while Henderson (1935), in
a comprehensive work on the nonmarine
Mollusca of North America places them
a little earlier. He reported that the
oldest known member of this group is
Goniobasis multicarinata Russell, which
was found in Alberta, and which is
believed to have existed during the
Lower Cretaceous. He listed other fos-
sil pleurocerids as follows: 13 species
from the Upper Cretaceous, 10 from
the Lower Cretaceous, and 28 from
the Cenozoic (Tertiary) era.
The species Goniobasis livescens and
Pleurocera acutum tvactum were
reported by F. C. Baker (1902) from
the Pleistocene loess. The oldest fos-
sil specimen of G. livescens, according
to F. C. Baker (1920), was found in
the Toleston deposits of glacial Lake
Chicago, whereas the oldest P. acuta
(quoted as P. subulare (Lea) were from
the Wabash and the Sangamon inter-
glacial deposits. Wright (1932) studied
post-glacial fossil remains of P. acuta
and G. livescens in the Tippecanoe
River system of Indiana and his find-
ings indicated that they had migrated
there from the Kankakee and Iroquois
Rivers at the close of the glacialperiod.
At present, the Tippecanoe system is
a tributary of the Wabash River and a
portion of the Ohio River drainage sys-
tem, where these snails still flourish.
Two conflicting ideas exist with regard
to the geographic origin of the living
members of this group. The first and
more popular theory supports the view
that the Pleuroceridae originated from
the Laramie formation (probable beds
in Colorado, Wyoming, Montana, Alberta,
and Saskatchewan). Their surviving des-
cendants are believed to have migrated
from the west to the Mississippi Valley
and southeastern United States together
with the Unionidae. This theory was
propounded by White (1882) who reasoned
that although the large lakes, which
existed in the Tertiary and Laramie
periods, successively became obliter-
ated, it was reasonable to conclude that
at least part of the river channels of
today have existed as such from earlier
geologic times. This applies to some
of the present tributaries of the Mis-
Sissippi River system that partly coin-
cide with former outlets or inlets, or
both, of these ancient lakes. It is pos-
sible, therefore, to infer that the mol-
luscan fauna of the Mississippi River
system descended directly from the
faunae of those ancient lakes and mi-
grated through the river systems in
which they constituted lacustrine
elements. Simpson (1896) accepted this
theory.
The opposite view tends to support
the idea that pleurocerids originated in
the southeastern United States and that
they spread westward, as they did during
more recent post-glacial migrations
(Walker, 1900). Adams (1915) favored
this theory, stating that the southeastern
streams have been favorable as habi-
tats for certain mollusks since the close
of the Paleozoic era. The presence
of a large number of endemic species
which are confined to that region
strengthens his view. He postulated
that the lack of fossils in the south-
east was brought about by the persis-
tent adherence of rivers to their ancient
channels; it is only in deposits of lacus-
trine portions of ancient river systems
that these faunal elements have been
preserved.
Geographic Distribution.
Lake Erie is the type locality for
Pleurocera acuta. Its general distri-
bution (Fig. 1) includes the headwaters
of the Ohio River and its tributaries,
the Mississippi River westward to
eastern Nebraska and Kansas. The
PLEUROCERA AND FONIOBASIS 11
species invaded the Erie Canal and en-
tered the basin of the Hudson River.
According to F. C. Baker (1928a) the
easternmost locality record for P. acuta
is a tributary of Lake Champlain in
Vermont, in the St. Lawrence drain-
age; the most northern locality recorded
is Lake Superior, Bayfield, Bayfield
County, Wisconsin. Some forms, in-
distinguishable from P. acuta, have been
taken as far south as the branches of
the Cumberland and Duck Rivers of
Tennessee (Goodrich, 1940) and the
tributaries of the Mississippi River
in Louisiana and Arkansas.
Goniobasis livescens is generally dis-
tributed from New York to the Great
Lakes region, and from Canada to the
Ohio River drainage (Fig. 2). It was
named and described by Menke in 1830,
from specimens collected from the
eastern end of Lake Erie. It is found
in the tributaries of the Ohio River,
east of the Scioto River in Ohio, the
Wabash River and its tributaries west
to the Illinois River; it is especially
common in the St. Lawrence River
basin, including the Great Lakes. G.
livescens occurs as far east as Lake
Champlain and parts of Quebec. It
also invaded the Hudson River Basin
by way of the Erie Canal. It has
been found in all of the Great Lakes
except Lake Superior though it is known
to occur in one stream tributary to
Lake Superior and within less than a
mile of the stream’s discharge; it oc-
curs also in the St. Mary’s River con-
necting Lakes Superior and Huron. In
the Ohio River drainage it occupies small
streams of western Pennsylvania and
various rivers in Ohio, excepting the
Scioto and the Little and Big Miami.
Somewhat the same discontinuous dis-
tribution is found in Indiana where G.
livescens lives in streams flowing into
Lake Michigan, in the Lake Erie drain-
age and the Wabash River with its
northern tributaries; it has not been
found in the White River forks, nor
in streams to the east of the Wabash,
such as the Big Blue and White Water
Rivers. Specimens were reported from
Des Moines River in Iowa by Goodrich
(1940). Baker (1928a) stated that in
Wisconsin С. livescens is confined to
Lake Michigan and streams emptying
ato it: The distribution of G.
livescens in Michigan, based on studies
by Goodrich (1945), is shown in Fig. 3
and the recorded distribution of P.
acuta in Fig. 4. It is evident from
these maps that G. livescens has a
wider distribution in this state than does
P. acuta. Goodrich (1940) further stated
that it had a wider distribution in
Michigan than any other aquatic mol-
lusk, with the possible exception of the
pulmonate, Helisoma trivolvis Say).
METHODS AND TECHNIQUES
Sampling Methods.
This investigation was begun with a
general survey for areas positive for
pleurocerid snails. Various collecting
sites were chosen in Michigan (and also
Ohio). For ecological and life history
studies, 4 permanent stations were
designated in 2 rivers and 2 smaller
streams near Ann Arbor, Michigan,
which are described in detail in the
Ecology section (p 41).
These stations were visited at least
once a month for a period of 1 year.
The snails were collected by 2 methods:
random sampling outside of the im-
mediate station area and quantitative
Sampling in staked areas.
In this second method, 3 one-meter
quadrat samples were taken at each
monthly collection, 2 samples on each
side of the stream and the third in
the middle. In order to avoid col-
lecting in the same place, successive
monthly samples moved progressively
to an up-stream undisturbed portion.
The quadrat area was staked by using
4 strips of tin-aluminum metal alloy
(each measuring 3 cm by 100 cm),
with holes drilled at each end. Iron
nails 6 inches long were driven through
the holes, marking the square meter
12 B. C. DAZO
enclosure. The tin-aluminum alloy is
heavy, sinks readily in water, and can
be clearly seen. The metal strips
also have the advantage of being easily
rolled and stored when not in use.
All snails visible within the sample
area through a glass-bottom viewer,
were removed with a pair of forceps.
Then the surface sand and gravel were
carefully scraped and shoveled into a
clean wooden box the bottom of which
was lined with fine (about 1 mm) wire
mesh for collecting the tiny snails.
Occasionally, when the snail density was
high only 1/2 or 1/4 of the quadrat
was sampled.
Most of the snails recovered in the
field were taken to the laboratory where
they were relaxed and fixed (see p 14-
15). Some were crushed on the spot
with a pair of pliers and fixed immedi-
ately in Lavdowsky’s Solution (Formalin-
Alcohol-Acetic Acid 2:10:1 parts by
volume) to preserve the stomach con-
tents for a study of the food habits
of these snails (see p 64).
Shell measurements were made for
use in a growth and life history study
(p 63 and Table 12). The data re-
corded were: (1) maximum length of
shell; (2) greatest width perpendicular
to the long axis; and (3) the number
of whorls present. Larger snails were
measured with calipers, whereas an ocu-
lar micrometer and a dissecting micro-
scope were used on the smaller ones.
In all cases, measurements were taken
with the aperture of the snail facing
the observer.
The sex of the snail was also deter-
mined (see p 63 and Table 13).
Limnological Methods.
Just before collecting snails at each
permanent station during the monthly
sampling, and at other collection sites
limnological and other ecological obser-
vations were made. The data taken
include: free carbon dioxide content
of the water, methyl orange alkalinity,
dissolved oxygen, pH, water current
velocity, water level fluctuations, tur-
bidity, and temperature records of both
the water and the atmosphere. Lim-
nological methods followed are those
presented in Welch (1948) and in the
“Standard Methods” of the American
Public Health Association (1955).
Ambient and water temperature were
taken with an ordinary mercury ther-
mometer. Water level fluctuations were
recorded as follows: a wooden post
was driven into the stream bed in the
middle of the stream and, using this
post as reference, the water depth was
recorded at each visit. A portable
Beckmann pH meter (Model 180) was
used for determining the hydrogen-ion
concentration of the water. This meter
was calibrated from time totime against
a standard laboratory apparatus. Water
current was determined with the aid of
a “pygmy” model current meter (Bat-
tery operated, serial number R-318),
manufactured by Arline Precision
Instruments, Baltimore 29, Maryland,
which had been calibrated by the U.S.
Bureau of Standards and Measures. The
free carbon dioxide content of the water
was taken in the field using phenol-
phthalein indicator and a N/44 aqueous
solution of sodium hydroxide as titrating
agent.
Methyl orange alkalinity was deter-
mined in the laboratory from 2 sam-
ples for each station. Two drops of
methyl orange indicator were added to
a 100 ml sample which was titrated
against an aqueous solution of N/50
Sulphuric acid until the water changed
from orange to a permanent light pink
color. The amount of sulphuric acid
used in cu. mm multiplied by 10 gives
the methyl orange alkalinity of the water
in parts per million (ppm). Two water
samples from each station were also
used for determining the oxygen content.
These samples were “fixed” in the
field using the H. Pomeroy-Kirschman-
Alsterberg modification method, as fol-
lows: 1 ml of potassium fluoride was
added to a 200 ml sample and agitated;
2 ml of concentrated sodium iodide and
2 ml of manganese dioxide solutions
PLEUROCERA AND GONIOBASIS
were added and mixed. A brownish-
red precipitate appears but is dissolved
by the addition of 1 1/2 ml of con-
centrated sulphuric acid. The fixed
sample was titrated in the laboratory by
means of an aqueous solution of N/100
sodium thiosulphate, until the color of
the water sample changed from orange
to light pink. The amount of sodium
thiosulphate used in ml multiplied by
the factor of 1.6 gives the amount of
dissolved oxygen of the water in parts
per million.
Maintenance in the Laboratory.
At the beginning of this program it
seemed impossible to maintain or cul-
ture pleurocerid snailsinthe laboratory.
The adults would survive for a few
days or weeks and then die out. Only
after more than a year of experimenting,
was it found that unless exceptionally
good oxygenation was supplied and un-
less adequate amounts of green algae
and diatoms were present, the pleuro-
cerids would not thrive. When these
two important needs were met, and
combined with periodic renewal of the
setup, the culture of these snails be-
came possible.
The pleurocerid snails were success-
fully cultured in two ways: in an arti-
ficial stream and in aquaria. The
artificial stream was made of 2 long
wooden troughs each 11 feet long, 12
inches wide and 6 inches deep, con-
nected at one end by a short trough
(29 inches) to form a U-shaped canal.
Leakage was prevented by lining the
corners and the bottom with fiberglass.
This set of troughs was set on a regu-
lar laboratory table with one end higher
than the other. The flow system was
completed by means of a plexiglass
paddle wheel mounted on a short end
trough at the lower, open, end of this
canal. A small electric motor attached
to the wheel served to move the water
from the lower end of the trough to
the upper, through a fiberglass channel,
creating a continuous flow without a water
tank or reservoir. Care was taken
13
to use neutral materials and to avoid
metal (especially copper) parts since
various metal ions are detrimental to
the snails.
River water, rocks, sand, soil and
water plants from the field were placed
in this artificial stream, to simulate
natural conditions. The troughs were
covered with glass to prevent excessive
evaporation of water and the water was
kept at a fairly constant depth of about
5 inches.
After trial maintenance runs, gravid
snails were transferred to this indoor
station. Oxygenbubblers were connected
at several points along the stream to
augment the aeration of the water. The
temperature of the water fluctuated, but
was near that of the outside atmosphere
because the windows were kept open
throughout the year. Natural light also
came from these windows.
This artificial stream served well for
some time. Later, the wood warped
on the side of the paddle wheel, which
was replaced by a small Bro-Jo Plastic
Pump. It successfully pumped water
from the lower to the higher side, and
no further difficulties were encountered.
Pleurocerid snails were also main-
tained and cultured in the laboratory in
regular aquarium tanks. These were
placed on shelves in front of windows
for sufficient lighting. Again water,
aquatic plants, rocks, soil, and sand
used in these tanks were taken from
the field. Oxygen was supplied to the
bottom of each tank by the usual aquar-
ium air bubblers. Eachtank was covered
with a glass lid. The water temperature
was 220 to 23° C (72° F) all year
round.
In both methods the pH was kept
within the range of 8.0 to 8.4; the
carbon dioxide and dissolved oxygen con-
tent of the water in the tanks were
checked at least once a month. Loss
of water by evaporation was unavoid-
able, even with glass covers, and in-
creased the salt content of the water.
In time, the increasing amount of fecal
materials also produced an increase in
14 B. C. DAZO
hydrogen-ion concentration. These ten-
dencies were offset by adding distilled
water. If, however, the pH fell below
8.0 either pond water was added or,
to increase alkalinity, calcium in the
form of powdered calcium carbonate and
calcium sulphate.
Adult female specimens ofboth species
were collected during spring and early
summer. They oviposited in the labora-
tory and many young hatched. Although
there was a high mortality rate among
the juvenile snails, many of them did
reach maturity and in turn laid eggs,
completing the cycle.
The snails were fed regularly with
fresh leaf lettuce. Other leafy vege-
tables, such as water-cress, spinach,
cabbage, etc., were tried but the snails
seemed to prefer lettuce. The Lee and
Lewer’s (1956) modification of the Stan-
den snail food (Cerophyll), which has
been used successfully with some planor-
bid snails, did not attract pleurocerids.
The diet was supplemented with green
algae and diatoms by providing rocks
and pebbles covered with green algae
and diatoms from the normal habitats
at least once a month; those previously
procured were then removed to avoid
overcrowding. Filamentous green algae
(Spirogyra) and blue green algae (Ana-
baena) often grew profusely and proved
to be a nuisance: the former is seldom
eaten, the latter is toxic, and both were
periodically removed to avoid crowding
the containers.
Because of the presence of one dead
Snail could induce fatalities among the
rest of the animals in the tank, dead
animals were immediately removed from
the culture. When a tank became too
dirty, with an overaccumulation of fecal
material, with the snails dying and a
consequent bacterial content, it was
completely reestablished.
When conditions in the tanks became
unhealthy ostracods would often appear
in great numbers and could often be
seen observed biting and attacking weak
snails. They always swarmed over the
decaying animals. A tank in which most
of the snails died was always one con-
taining a thriving colony of ostracods.
Leeches and planarians were often seen
within the shells of decaying animals.
Care was therefore taken to keep the
aquaria fresh and to avoid proliferation
of the scavengers. The common aquari-
um fish Lebzstes reticulatus (Peters)
was not kept in the snail tanks after
observing that it would eat the eggs of
pleurocerid snails.
With the methods outlined above,
pleurocerid snail culture in the labo-
ratory was very successful and it was
now at last possible to initiate studies
on egg-laying activities, mating and
feeding habits and longevity. Success in
culture likewise insured a good supply of
normal specimens for basic work in
morphology, for most pleurocerid snails
collected in the field were heavily para-
sitized by larval trematodes and there-
fore not considered representative.
Preparation of Materials for Anatomical
Studies
The snails to be studied were placed
in finger bowls or white enamel pans
containing pond water (usually 150-200
cc). They were relaxed by adding a
few menthol crystals. The container
was then covered with a glass plate.
In this initial stage extreme care must
be taken not to shake or move the con-
tainer because the animals are very
sensitive to such stimuli and contract
immediately. Once contracted, they are
not apt to relax again. It usually takes
about 6-8 hours for the animals to
properly distend and relax with menthol.
After that time, about 10 cc of 10%
veterinary sodium nembutal was added.
The total relaxation time was usually
about 16 to 18 hours. The animals were
then immediately fixed, either with
Bouin’s picro-formol solution or with
10% neutralized formalin. This timing
is important for obtaining good speci-
mens. If fixation is attempted before
the snails are completely relaxed, the
animals invariably pull back into their
shells and are fixed with their opercula
PLEUROCERA AND GONIOBASIS 15
closed. If however, the specimens are
fixed a few hours after complete relax-
ation, the soft parts show tissue wrinkles
and partial disintegration. Specimens
remained in the fixative for at least 24
hours but never beyond 72 hours. Longer
fixation produces tough and hard tissues
which are unsuitable for gross dis-
section. After fixation, the animals were
carefully removed from their shells,
transferred to 30%, 50% and finally 70%
ethyl alcohol solution.
Empty shells and opercula were
cleaned with a small brush using soap
and water. Shells were dried in air
and then stored for measurements.
Opercula were also soaked overnight in
a weak solution of oxalic acid, rinsed’
and again cleaned with a brush. Later,
they were passed through series of
alcohol solutions (30%, 50%, 70%, 85%,
95% and 100%). The opercula were
cleared with xylene and mounted in
Canada balsam.
For radular preparations the entire
buccal mass, including the radular
ribbon, was carefully dissected from
relaxed animals and soaked for a few
days in a weak solution of sodium
hydroxide to dissolve away the tissue.
Afterwards, the radular ribbon was re-
moved carefully and washed in a 10%
acetic acid solution to neutralize the
hydroxide. The ribbons were then washed
in distilled water and passed through
increasing grades of alcohol. Prior to
staining and mounting, they were stored
in 70% alcohol. Some radulae were
stained with Orange G using Roger’s
(1924) electrical method. Most of them
were stained with chromic acid, borax
Carmine, and eosin. The ribbons were
transferred from 70% alcohol to the
stain. It was found helpful to overstain
and then destain slowly in acid alcohol
(70% with a few drops of concentrated
hydrochloric acid) transferring toa basic
alcohol to the desired intensity. After
washing the ribbons in a neutral 70%
alcohol, they were dehydrated with in-
creasing grades of alcohol through 100%
and cleared in xylene. They were then
carefully flattened on a microscope slide
and mounted in Canada balsam or
euparal. Some were ripped apart with
teasing needles before mounting on the
slide to allow a better view of individual
teeth.
The jaws were carefully dissected
from the buccal mass, cleaned and
stained with aceto-carmine, prepared in
a similar manner and mountedin Canada
balsam.
Whole mounts were prepared as
follows: the newly relaxed and unfixed
animals were held between two glass
slides. Gentle pressure was applied to
the slides and, at the desired thickness
they were bound into position with a
piece of string. The preparation was
then fixed for at least 48 hours in
formalin or Bouin’s. According to the
fixative used they were either washed in
running tap water to remove all traces
of formalin or to hasten the removal
of excess picric acid in finger bowls to
which a small amount of powdered lithium
carbonate had been added. The washed
specimens were then passed through in-
creasing grades of alcohol to 70%. They
were stained in borax carmine. Over-
stained specimens were slowly destained
in acid alcohol as indicated for the
radulae. The stained specimens were
dehydrated in alcohol and cleared in oil
of cloves. The excess oil was removed
with xylene. The whole mounts were
made with Canada balsam. Pieces of
broken glass were used to support thick
specimens in these slide preparations.
Gross dissection of preserved speci-
mens was done under a dissecting micro-
scope in dishes partially filled with wax
on which the specimens were mounted.
The preferred dissecting fluid consisted
of equal parts by volume of pure glycerine
and 70% alcohol. The fluid made the snail
tissues soft and quite pliable. Pliers
were necessary for Cracking and re-
moving the hard calcareous shell of the
animal; jeweler’s or watchmaker’s
forceps, scalpels with pointed ends,
scissors with curved tips, extra fine
insect pins, fine camel hair brushes and
16 B. C. DAZO
other standard laboratory supplies were
used for detailed dissection. Nervesand
delicate membranes were traced by
means of a 0.5% aqueous solution of
methylene blue dye (Basch, 1958).
Formalin (15% solution) was used to
remove excess dye in the nerve tissues;
a neutral 70% alcohol removes the blue
dye completely from all tissues.
For vivisection sometimes the snails
were first anesthetized in menthol and
the shell was then removed with a pair
of pliers. Dissection was carried out
in physiological salt solution developed
by Fraser (Carriker, 1946).
Histological Methods
Serial sections were made ofthe whole
animal as well as of excised organs and
organ systems. Most of these prepa-
rations were made with animals whose
shells had been removed with Bouin’s
picro-formol solution; some were of
animals carefully extracted from their
Shells. The fixed animals were well
washed in running tap water to remove
excess picric acid. The specimens were
then passed up through the alcohol series
to absolute alcohol. They were cleared
by passing through a solution of 1:1
chloroform andabsolute alcohol and were
later transferred to pure chloroform.
Wax infiltration began at the half chloro-
form and half paraffin stage. After about
30 minutes, the specimens were trans-
ferred to pure paraffin for complete
embedding. The blocked paraffin tissues
were cut at 124. The sections were fixed
on the slides with egg albumen and the
ribbons were flattened on an electric
slide warmer.
Paraffin was removed from the slides
by immersing them in 2 changes of
xylene. The sections were then run
through a decreasing series of alcohol
to 30% and finally to water. The tissues
were stained with hematoxylin (Harris
and Ehrlich’s acid hematoxylin) and
washed in tap water. After staining, the
slides were passed through anincreasing
series of alcohol to 95% and counter-
stained with 0.5% Eosin for 30 seconds.
After washing the slides several times
in 95% alcohol, they were dehydrated in
absolute alcohol, and cleared in oil of
cloves and xylene; mounts were in
Canada balsam or euparal.
The histological and embryological
photographs (Plates VI and VII) were
taken with an Exakta VX Ila, a single-
lens reflex camera. The morphological
drawings were made with the aid of a
camera lucida at table height.
MORPHOLOGICAL STUDIES
Shell and operculum
As previously stated, most of the
literature available on pleuroceridae
deals with the shell and its variations.
Little is to be added to the innumerable
papers on shell characters. The brief
description given here is based on publi-
cations by F. C. Baker (1902, 1928a)
and Calvin Goodrich (1939c, 1945), both
of whom adequately described the dextral
shells and the opercula of P. acuta and
G. livescens; it is supplemented by
observations on the material used in
this study.
Pleurocera acuta
Shell. The shell of this snail is thick
and heavy, somewhat conical in shape,
and much elongated (Plate I and Fig. 11).
The color of the shell varies from pale
brownish horn to dark chestnut. Black
and pale yellow specimens are also
found. In nature, the shell is often
coated with mud or algal growth. When
cleaned, some have a lustrous surface,
while others may appear dull. In river
forms, a yellowish band sometimes en-
circles the whorls just below the suture.
In some lake forms, 2 or 3 brown bands
often are clearly visible on the inner
and outer side of the body whorl.
Oblique lines of growth and prominent
scars often appear on that whorl. It
is angulate, with or without sharply
defined carinae. A double carina or
ridge tends to be very distinct in the
young. This carinationis usually carried
PLEUROCERA AND GONIOBASIS
17
4
PLATE I. Pleurocera acuta andGoniobasis livescens as they appear in the living condition
and their opercula (insets).
FIGS. 1&2. P. acuta FIGS. 3&4. G. livescens
18 B. C. DAZO
only on the first 3 to 6 apical whorls
in adult shells, while the later whorls
appear smooth. The median ridge or
carina is more prominent than the one
located near the suture. Occasionally
one encounters a shell with 1-3 carinae
encircling the base of the body whorl.
The shell of an adult is 29.92 mm long
on the average and 11.29 mm wide (See
Table 13). It usually has 9 to 11 whorls
but in unbroken specimens the number
may go to 15. The shell aperture is
subrhomboidal, white, bluish-white to
purple within, angulate, tending to form
a canal below (canaliculate). The
columella is twisted, with a bluish-
white tint.
Operculum (Plate I, Fig. 2). The
paucispiral operculum is chitinous, thin
and reddish-brown in color. There are
3 opercular whorls in the adult. It is
somewhat oval in shape with the left
margin almost straight and the basal
and right margins broad and regularly
curved. Its apex is more or less
roundly acute. The growth lines are
fine and numerous and the rest scars
are very well marked by darklines. The
nucleus is sunken and located at about a
third of the distance from the base to
the apex, nearer the left margin. The
area of attachment to the columellar
muscle of the foot occupies about half
the anterior (=nuclear) side.
An interesting observation on the oper-
culum of P. acuta was made by the writer,
which agrees well with those made by
Goodrich (1939a) in Pleurocera canali-
culatum undulatum and in other pleuro-
cerids. In the laboratory some of the
animals were noted to lose their oper-
cula. This loss seemed to be brought
about by encysted parasites (ostracods?)
that were often seen occupying the region
between the base of the foot and its
attachment with the operculum. An
entirely new operculum then grows to
replace the missing one. At first this
new structure was extremely thin, though
full size. Within 3-4 months the new
operculum attained the normal thickness
and texture.
Goniobasis livescens
Shell. According to Goodrich (1939c)
this mollusk shows extreme variations.
He reported that the spire may be long
or short and loosely or tightly coiled;
whorls flattened to rounded; shell shape
slender and elongate to ventricose.
These extremes in variation were also
exhibited among specimens collected
from all 4 study stations sampled inthis
study.
Adult shells of G. livescens are
ovately-conic, elongated and often
turreted on the upper whorls. They
average 18.24 mm in length and 8.79
mm in diameter (See Table 13). The
juveniles, on the other hand, are conic
or pyramidal and the carinae are promi-
nent structures in both spiral and body
whorls. Specimens collected at the
Zuckey Lake Inlet Station had the fine
carinae on the juvenile whorls continued
as strongly marked keels on the mature
whorls (Plate I and Fig. 11).
In the other 3 permanent collecting
stations, however, this carination was
usually wanting because of the eroded
condition of the adult shell. If present,
it was found only in the first 2-3 apical
whorls. The apex or nucleus is seldom
present. The body whorl is usually
convex and inclined to be bulbous.
The shell is smooth. Its color varies
and may be bluish-gray, light or dark
brown, plain black, greenish light
yellow or flesh color. It is for the
“bluish” specimens that Menke (1830)
selected the specific name “livescens”:
(from (lividus = blue). A greenish or
yellow green hue is apparently due to
algal growth. Goodrich (1939c) attri-
buted the dark brown or black coloration,
which is characteristic of most streams
of Upper Michigan, to “bog stain”. This
dark color contrasts with that of the
shells of downstream and lake colonies,
which are yellow or light brown. A
light yellow band may encircle the whorls
just below the suture.
Adult shells of G. livescens have 7 to
9 whorls; specimens of the same age
PLEUROCERA AND GONIOBASIS 19
appear to have the same number of
whorls, although their size varies
greatly. Shells taken at the Lake Erie
station are nearly twice the size of
specimens collected from Zuckey Lake
Inlet station (Table 13). The number of
whorls serves as an excellent index for
comparing snails of various sizes and
shapes but evidently belonging to the
same age group. The whorls of older
specimens are usually flat-sided while
those belonging to immature shells are
convex, bulbous or rounded.
The aperture of С. livescens is large,
less angulate than that of P. acuta and
without the basal canal. It is ovate or
subrhomboidal, somewhat produced at
the lower part and in live specimens of
a brownish-purple to purple color inside.
The peristome is sharp, thin, but thick-
ened with a callus within the outer lip,
and more or less sinuate. The columella
is thick, smooth, not twisted and tinged
with blue or purple.
Operculum. The operculum of С.
livescens is chitinous, thin, ovate, and
reddish brown. It has 3 whorls in the
adult. Its shape is similar to that of
P. acuta except that its apex is more
acute (Plate la, Fig. 4). The growth
lines are coarse in G. livescens; under
a microscope they appear as very fine
wavy lines with wrinkled ridges. Growth
lines or rest scars are more prominent
than in P. acuta. By an analysis of
these scars, it might be possible to
determine the age of this species with
some degree of accuracy. As in P.
acuta, the nucleus is sunk; it is located
at the lower quarter or third of the
long diameter, near the left margin. The
area of attachment of the columellar
muscle occupies the upper 2/3 of the
length of the operculum and the right
edge of the ihner side.
Trunk Region
Head-Foot Region. A general aspect
of this region is shown in Plate I
and Text Figure 5. Usually an adult
P. acuta is about twice the size of С.
livescens. My observations lead me to
agree, in the main, with the descriptions
given by F. C. Baker (1928a) and Good-
rich (1945), although some oftheir state-
ments, especially those referring to
coloration, are not representative and
need correction.
F. C. Baker (1928a) described P.
acuta as follows: “Animals with wide,
Short, thick foot, truncated before and
rounded behind; color blackish above,
yellowish underneath; the top of the
rostrum is marked by black transverse
bands or spots; side of the body and
foot streaked with black; mantle dark
gray or blackish; operculigerous lobe
conspicuous; head prominent, with large,
somewhat elongated proboscis or
rostrum, subconical in form, which is
capable of considerable extension when
the animal is in motion; mouth placed
at tip of rostrum, disk-like, and repre-
sented by a long longitudinal slit which
divides the snout-like end into a double
disk; the radula may be plainly seen
in the mouth when the animal is feeding;
tentacles rather long, tapering, very
narrow; eyes black, placed on swelling
at the outer base of the tentacles;
mantle simple, folded on the right side
to form the respiratory cavity; on the
right side of the body there is an
impressed line which extends along the
body in a parallel direction and curves
to the margin of the foot behind the
right tentacle; gills as usual in this
group, the primary gill being very
narrow.” I have found that the foot of
P.acuta has a yellowish to grayish-
orange color; the orange hue becoming
more prominent on the margin. As
for С. livescens, he stated: “Similar
in form to Pleurocera. Body yellowish-
white with lines of black; orange or
yellowish on neck; rostrum orange near
tip, darker on upper part; under side
of foot bluish white, flecked with dark
spots. The whole body is sometimes
lemon-yellow.” However, there is no
question but that the head-foot region of
G. livescens is muchbroader and shorter
than that of P. acuta.
Calvin Goodrich (1945), on the other
20 B. C. DAZO
large intestine gills
stomach
digestive gland (liver)
small intestine
heart
kidney
PA
operculum
columellar muscle
mantle collar
efferent ctenidialsinus
right cerebral ganglion
tentacle
esophagus
radular sac
salivary gland
right pedal ganglion
foot
FIG. 5. Arrangement of organs in Goniobasis livescens. Lateral view (right side) with shell
removed. The osphradium, on the left inner side of the mantle, can not be seen.
hand, more appropriately described G.
livescens as follows: “The body of the
male specimen was rather short and
rounded posteriorly and had a blunt
wedge-shaped rostrum. The mouth was
a narrow, vertical slit. The tentacles
were short, thick at the base, and
tapering to a blunt termination. Strongly
pigmented eyes at the base of the
tentacles were conspicuous. The mantle
covered about three-fourths of the body;
its margins were smooth. Atrench-like
line extended from the pallial cavity to
the right tentacle. The color in general
was grayish to nearly black. A female
of the same colony, taken at the same
time, differed in showing faint discon-
tinuous stripes of tallowish coloration
on top, not greatly contrasting with the
leaden hue of the body mass. Irregular
spots occurred here and there on the
sides of the foot. Thetipofthe tentacles
was translucent, nearly colorless. In
the extended animal, the operculum
rested in a fold or pocket, showing only
its edges. The edges of the mantle
were slightly yellow.” However his
statements about sexual differences in
coloration and marking cannot be
generalized.
The rostrum of both species has a
pattern of black pigmented stripes
against a yellowish-orange background
resembling that of a tiger, only in finer
detail. These pigmented areas are
more prominent near the mouth and
diminish into spots near the neck of
the mantle region. The portion of the
rostrum which forms part of the mouth
and comes in contact with the surface
of the rocks and gravel when the animal
browsing has a bluish-yellow or bluish-
white color.
Mantle and its cavity. The mantle
surrounds the neck and head-foot region
of the snail. It protects the neck and
PLEUROCERA AND GONIOBASIS 21
the anterior organs, especially the head,
foot and sense organs. It also acts as
a buffer between the hard calcareous
shell and the animal itself, spreading
like a cushion throughout the entireinner
surface of the body whorl. It is inner-
vated by nerves coming from the anterior
portion of the cerebral ganglia and is
supplied with blood originating from the
ctenidia or gill sinuses. It is thin, white
and almost transparent. In live speci-
mens the mantle may be seen adhering
closely to the inner surface of the body
whorl. The collar or anterior margin
of the mantle is smooth and surrounds
the edge of the aperture.
The space between the neck, the head-
foot region, and the mantle is called the
mantle cavity. The gill filaments and
the osphradium are located inthis cavity,
as well as the termination of the genital
laminae and the anus.
Sense Organs
Eyes. The eyes of P. acuta and G.
livescens are located at the outside of
the slightly swollen base of the long
tentacles (Plate I and Text Figure 5).
They are innervated by the optic nerve
which originates on each cerebral
ganglion.
Otocysts (Statocysts). These organs,
one on each side of the animal, are
located below the pleuropedal commis-
sures on the postero-dorsal surface of
the pedal ganglia (Plate II, Fig. 3).
They appear as white spherical bodies
about 0.250 mm in diameter; they are
connected to the pedal ganglia by thin
connective tissues and minute nerves,
and are mainly innervated by the 2
statocyst nerves originating from the
cerebral ganglia. Their function is
generally thought to concern balance
(Tschachotin, 1908).
Osphradium. The osphradium (Text
Fig. 9 and Plate IV) is found in the
pallial cavity to the left ofthe ctenidium.
Although it is in the direct path of the
respiratory current, it is not thought to
have a respiratory function. Lacaze-
Duthiers (1859) speculated that this
gastropod organ had a sensory role.
Spengel (1881) reported that it served to
test the physical and chemical properties
of the water entering the pallial cavity
and that this might possibly aid in food
selection. Bernard (1890) supported
Spengel’s theory. Copeland (1918)
working ontwo marine gastropods proved
that the osphradium served as an organ
that assisted the process of procuring
food. More recently, Magruder (1935b),
in Pleurocera, verified that it does not
have any respiratory function.
Tentacles. In previous reports, the
tentacles have not been considered as
sense organs. Since they obviously serve
as organs of touch, it seems proper to
include them here. The tentacles (Plate
I and Text Fig. 5) are long and slender
extensions from the dorso-lateral
portions of the head. They have a
yellow or light golden color with black
pigmentation scattered to form a striped
pattern. The tentacles of P. acuta are
much longer and more tapering than
those of С. livescens. A longitudinal
section of the latter is shown in Plate
VIL ЕЕ 5.
Nervous System
Rosewater (1961) published ob-
servations on the nervous system of
pleurocerid snails. He found that the
central nervous system of 9 species of
North American Pleuroceridae differed
from each other mainly in the length
of the cerebral commissure and of the
length of the connective between the left
pleural ganglion and the subintestinal
ganglion. Since he used only 6 specimens
of each species, and since in my opinion
none of the specimens were properly
relaxed and fixed, it is doubtful whether
his data can be considered reliable for
detail.
Only one reference dealing in detail
with the central nervous system of a
pleurocerid snail was found in the
literature: Magruder’s (1935b) report on
Pleurocera canaliculatum undulatum.
To facilitate a comparative approach,
his terminology is used here for the
22 B. C. DAZO
various ganglia10 and nerves, as well
as his definition of commissures and
connectives, so that the nerves con-
necting like ganglia of opposite sides
are called commissures, whereas con-
nections between unlike ganglia of the
same or opposite sides are referred
to as connectives.
Comparing tue central nervous system
of P. acuta and G. livescens with that of
P. canaliculatum undulatum (Say) and
lo fluvialis (Say), a related pleurocerid
whose anatomy will be described and
published later, it was found that it is
essentially the same and differs mainly
in size. The general pattern appears,
on the whole, similar to that of other
Cerithiacea. These similarities are,
for instance, evident from the work of
Sunderbrink (1929) ор Melanopsis du-
Jourei Férussac and Cerithium vulgatum
Bruguiére, snails belonging to the related
families Melanopsidae and Cerithiidae
respectively. As an example of simi-
larity, the subintestinal ganglion in C.
vulgatum is also closely associated and
connected to the left pleural ganglion,
as it is in the melaniid genera Pachy-
melania, Potadoma and Cleopatra
(Binder, 1959). The position of that
ganglion differs, however, in Melanopsis
dufourei, where it is located between
the right and left pleural ganglia and
joined to them by long connectives.
Bright’s (1958, 1960) illustration of the
nervous system of Cerithidea califor-
nica (Haldeman) show that the following
features differentiate Cerithiidae from
Pleuroceridae: 1) the cerebral commis-
sure is lacking; 2)thereis no connection
between the subintestinal ganglion and
the right mantle nerve; and 3) the
visceral ganglion does not form a Y-
Shaped structure; instead, a widely
split or broad U-shaped connection is
formed between the right and the left
10He used the terminology applied to ganglia
by Spengel (1881) which is generally ac-
cepted.
visceral connectives from which 4 smal-
ler nerves branch off posteriorly.
п: the present work only the main
branches of the central nervous system
of P. acuta and G. livescens, have been
illustrated (Plate II, Figs. 1, 2 and 3).
Not only were the smaller nerve rami-
fications very difficult to follow but they
also vary considerably as to size,
number, and their relative position even
among individuals of the same species.
The central nervous system is com-
posed of 4 principal pairs of ganglia,
namely: the cerebral, the buccal, the
pedal, and the pleural ganglia with their
associated connectives. In addition,
there are 3 minor and unpaired ganglia;
the subintestinal, supraintestinal, and
the visceral.
The following account applies to both
P. acuta and G. livescens. For all
paired ganglia except the pleural, a
description of only one side will be given
since all of the nerves that originate
from them are paired and identical.
The pleural ganglia differ from one
another in size, shape and arrangement
of nerves and are discussed separately.
Cerebral Ganglia and their Nerves.
The most prominent pair of nerve centers
in the anterodorsal part of these snails
are the cerebral ganglia. They are
located on each side of the esophagus
and are more or lesstriangular although
somewhat flat. Their posterior ends are
directly dorsal to the extreme anterior
ena of the pleural ganglia. They form
a rooflike “canopy” over the esophageal
region. A total of 9 pairs of nerves
arise from the cerebral ganglia. The
anterior end of each ganglion is pointed
where it gives off 5 large nerves going
to the anterior head region and the
buccal mass. Each ganglion gives off 3
lateral nerves, one eachfromits antero-
dorsal, anterolateral and posteroventral
sides. From the mid-ventral surface of
the cerebral ganglion also originates the
nerve that forms the corresponding pedal
ganglion.
Toward their posterior end, the paired
cerebral ganglia are connected to each
PLEUROCERA AND GONIOBASIS 23
\
À
Ey
G
F 2
ES
Е
Z
Z
Е N tentacle
= labial nerves À
Z tentacular nerve [1
= 4
À
[a
cerebral ganglion
pleuropedal connective
left pleural ganglion
optic nerve E \ ; À
Z N FA
left pleural ganglion HO
left mantle nerve 7
right pleural ganglion
right mantle nerve
mantle
right pleural ganglion
nght mantle nerve
subintestinal ganglion.
supraintestinal nerve
genital nerve Subintestinal nerve
mantle Ne
supraintestinal ganglion
A
AWA Mn ks: I \
A
>
Nun El ;
\ N
left mantle nerve
0
A
KO
>.
=
7 - -
@ right visceral connective
Е
F .
visceral ganglion
visceral nerve
tentacular nerve
3 mantle
supraintestinal nerve Gy optic nerve
G a E :
27 à otocyst right pleural ganglion
=} у TR GEL
FG I cerebral ganglion
labial nerves
left mantle nerve
: <=: |
subintestinal nerve =x
subintestinal ganglion
I,
auricle 4
— 4 P” etterent
ur ctenidialsinus
ricle e
vent efferent renal sinus
Organs of the mantle region and other miscellaneous structures.
1. The mantle was excised and turned back toward the right to expose its inner side and
the various organs it contains. Magnification approximately 35X.
Gill leaflet with the blood vessel (right lower side) as it enters the gill.
The otocyst and its relation to the pedal ganglion.
2
3
4. The kidney with its many folds.
5. The heart.
rectum. Magruder (1935b) described
these sinuses in P. canalculatum un-
dulatum, and discusses the function as
follows: ‘‘Blood from various parts of
the body is finally collected into 2 main
sinuses - the perivisceral and peri-
intestinal sinuses, from which it returns
to the heart by one of the 3 general
routes: 1) directly to the afferent
ctenidial sinus by way of the perirectal
and mantle sinuses, and through the
ctenidium to the efferent ctenidial sinus,
thence to the auricle; 2) through the
anterior renal chamber and to the
afferent ctenidial sinus to follow the
same route; 3) to the posterior renal
organ by way of the afferent renal sinus,
through the renal plexus to the efferent
renal sinus into the auricle without
aeration.”
Excretory System.
In P. acuta, G. livescens and also Io
fluvialis, the kidney (Figure 8 (2))
is large, oblong and flat, and opaque
white to light gray. It is made up ofa
series of leaf-like fused lamellae and
covered by a thin layer of connective
tissue. It lies on the anterodorsal
surface of the proximal portion of the
intestine and is in close contact with
the anterior part of the stomach. In
females it is located immediately behind
the posterior region of the genital fold
and the seminal receptacle; in males
it is found behind the prostate gland.
PLEUROCERA AND GONIOBASIS 35
The gills or ctenidia are anterior to the
kidney. The pericardial sac containing
the heart lies posterior to it. Two
openings lead from the kidney: one to
the pericardial cavity, and the other to
the pallial cavity. It is probable that
the only means of eliminating metabolic
wastes is through these body cavities.
For the circulation of blood in the
renal organ see the vascular system
(p 32).
Histologically (Plate VI, Fig. 1), each
leaf appears spongy and vascularized due
to the loose arrangement of the glandular
cells. These are irregular in shape and
may be differentiated from the cells of
the gills (Plate VII, Fig. 6) by the
absence of cilia.
Further information was given by
Magruder (1935) in his description of
the kidney of P.canaliculatum undulatum
which also applies to the species here
studied.
Respiratory System.
The respiratory system consists of a
set of gills or ctenidial branchiae (Fig.
8 (1 and 2)). These arise as
folds from the mantle and appear to hang
from the roof of the pallial cavity. They
are arranged in one set or column in
the manner of a comb (=pectinibranch).
When the snail is held with a pair of
forceps and immersed under water, so
that the shell aperture faces the
observer, these gills are easily seen at
the back of the head somewhat on the
left side of the anterior part of the inner
side of the mantle. The middle gills
are more or less triangular in shape,
and fairly uniform in structure, although
they vary in size. Those located near
the anterior and posterior end of the gill
column are much smaller and irregular
in both size and shape.
In Pleurocera acuta there are about
102 to 110 gills in a set and in Gonio-
basis livescens 75-87. The middle gills
measure 1.80 by 1.53 mm for P. acuta
and 1.50 by 1.18 mm for G. livescens.
Histological sections of the gills are
Shown in Plate VI, Figs. 4 and 6.
Reproductive System.
The pleurocerids, like the proso-
branchs in general, are dioecious. Ex-
cept for one subfamily, the males lack
external genitalia. For this reason
difficulties were encountered in dis-
tinguishing the males and females in
the Pleurocerinae. Stimpson (1864) was
the first to observe a deep pit or sinus
in the neck, between the right tentacle
and the foot, in the females of 2 species,
Mudalia dissimilis and Melania (-Gon1o-
basis) virginicall. F. C. Baker (1902,
1928a) did not succeed in differentiating
the sexes of Pleurocera subulare
@Pleurocera acuta) and Goniobasis
livescens on this basis, since he stated
that the only wayto determine the sex was
to crush the animal and examine it for
Ova or spermatozoa under a microscope.
Later authors have consistently found
this reproductive “ovipositor” pit and
some have described a transitional,
functional egg-laying groove leading to
this pit from the mantle cavity, and the
presence of a rudimentary papilla near
the pit. Moore (1899) is of the opinion
that the reproductive grooves and
pouches of the “Melanians” are to be
regarded as extremely primitive charac-
ters and are to be looked upon as the
last remains among existing Proso-
branchia of the grooves andintroversible
penes of the Opisthobranchia. To
strengthen his point, Moore cited the
case of the female Littorina and some
other forms, such as Strombus, whose
part of the accessory reproductive
apparatus, the groove, still remains,
albeit it appears to have no function.
Having examined several thousand
pleurocerid snails belonging to 6 genera
and 19 species or forms, the writer
has also found the sinus a reliable
character for differentiating the sexes
in this group. These pleurocerids are:
Io fluvialis brevis, lo f. lyttonensis,
Не regarded the 2 species as identical be-
cause of the basic similarity in their
anatomy.
36 B. C. DAZO
Pleurocera acuta, P. canaliculatum, P.
с. undulatum, P. curtum, P. unciale, P.
unciale curtatum, P. subulaeforme,
Goniobasis livescens, G. clavaeformis,
С. arachnoidea, С. proxima, С laqueata,
G. mutabilis, G. virginica, Anculosasub-
globosa, Eurycaelon anthonyi, and Nito-
cris (Anculosa) carinata. The groove
was present in live material and in all
relaxed females of P. acuta and G.
livescens used for dissections. A
papilla-like structure in the vicinity of
the pit was observed only in a limited
number of specimens.
Serial sections of the gonads of these
2 species were prepared and examined.
No evidence was found to indicate herma-
phroditism. The presence of larval
trematodes in the gonads was ascer-
tained.
Data on the reproductive system of
Pleurocera and Goniobasis are available
in the literature. Jewell (1931) studied
serial sections of G. livescens correcta
and made observations on reproduction,
but did not attempt to describe the
general morphology of the reproductive
organs. Woodard (1934, 1935, 1940),
however, in his work on G. laqueata
gave an excellent description of the
reproductive system of that animal and
described its eggs and egg-laying habits.
He also thoroughly discussed the struc-
ture and function of typical and atypical
Spermatozoa. Magruder (1935b) de-
scribed the reproductive system of P.
canaliculatum undulatum.
In pleurocerids, the genital tract, in
both sexes is composed ofa “closed”
initial portion and an “open” or laminal
terminal portion.
Male Reproductive System
Excepting for size, the system is
identical in P. acuta and G. livescens.
It consists, in the closed tract, of: the
testis, sperm duct, prostate, cytophore
and, in the open tract, lateral (left)
lamina, medial (right) lamina, spermato-
phore organ and the genital canal or
12Woodard’s (1934) terminology.
groove (Text Fig. 9). The sexual products
are the sperm and spermatophores (Plate
IV).
(1) The testis is one of the largest
organs in these snails. It occupies most
of the shell region above the body
whorl and surrounds the digestive gland
(liver) excepting for a narrow strip on
each side of the genital duct. On the
surface, the testis is lobate and com-
posed of numerous branched, tubular
follicles. The color is a light or pale
yellow, which, during the breeding season
becomes golden yellow due to the
presence of pigmented granules in the
ectodermal covering as described by
Woodard (1935) for Goniobasis laqueata.
Its tiny tubules anastomose to form
common tubes, the vasa efferentia.
(2) All of them empty into a common
duct, the sperm duct. This duct runs
along the columellar side of the coiled
liver and testis, together with the
visceral artery and a nerve from the
visceral region, until it reaches the
antero-ventral portion of the style-
sac or the stomach. It then curves
abruptly before it terminates at the
pocket-like structure formed by the end
portion of the open tract where the
medial lamina folds over the lateral
lamina.
(3) After this end point of the closed
genital system and just below the
beginning of the open genital canalisa
much folded, thin walled structure, which
Woodard (1934) called cytophore in
Goniobasis laqueata.
(4) He also referred to the terminal
portion and more dilated area of the
sperm duct near the open genital tract,
as the prostate.
(5) Beyond the prostate, the genital
groove extends forward as 2 broad
laminae fused dorsally to each other and
to the mantle. The ventral margins of
the laminae are free, forming a slit-
like channel between them, which commu-
nicates freely with the mantle cavity.
This channel is the only opening in the
male tract and the sexual products are
discharged freely into the general mantle
PLEUROCERA AND GONIOBASIS 37
prostate
spermatophore organ
gills
anus
eo : osphradium
= mantle ad
digestive gland (liver)
sperm duct
py testis
cytophore organ
lateral lamina
medial lamina
rectum
oviduct
seminal receptacle
nidamental gland
ee y
FIG. 9. The reproductive system of Pleurocera acuta. The head-trunk region was removed
and the mantle was cut on the left side and turned back toward the right to expose its inner
side. Approximately 20X.
cavity. The epithelial lining of theinner
wall of the posterior portions of the
laminae has numerous folds creating
pockets. According to Woodard (1935) the
membranous spermatophores (see
below) are formed in these pockets
around the masses of spermatozoa
passing through and he consequently
designated this portion of the laminae
as the spermatophore organ (Text Fig. 9).
It is believed that, in the absence of
copulatory organs for direct transfer
of sperm, the spermatophore is a pro-
tective measure for the preservation
38 B. C. DAZO
and storage of sperm.
(6) As inG. laqueata and P. canalicul-
atum undulatum, the spermatozoa found
in P. acuta and G. livescens are of
two types (Plate IV, Figs. 1 and 2),
namely, the typical “eupyrene” or “hair-
shaped” forms and the much larger
atypical “apyrene” or “worm-shaped”
sperml3, both of which are formed by
the primordial spermatogonia. Woodard
(1935, 1940) gave anexcellent discussion
on the spermic dimorphism in G.
laqueata. In the forms he studied (1934),
namely: Io, Anculosa, Gyrotoma,
Pleurocera, Goniobasis and Lithasia, he
stated that “there are no differences to be
observed between the typical spermato-
zoa, and the same may be said for the
atypical.” He indicated that the normal
eupyrene spermatozoa are enclosed in
spermatophores while still in the male
reproductive tract and that the atypical
apyrene spermatozoa which make a de-
layed appearance in the testis, are never
included in these spermatophores (see
under 7, below) and hence never reach
the females, and suggested that these
bodies perhaps did not have a necessary
functional relationship to the ova or to
the eupyrene spermatozoa. Regarding
the chromosomes of G. laqueata, Wood-
ard reported a haploid number of 18
in the first maturation division of a
typical sperm and the absence of hetero-
chromosomes.
(7) A spermatophore of G. livescens
is shown in Plate IV, Fig. 3. Itis a
crescent-shaped hollow sac whose tips
are spread out then folded back slightly
toward the convex side. Itis 4.5mm long
and 1.5 mm at its widest diameter. In
the spermatophores the sperm cells do
not follow a definite pattern of arrange-
ment. Only typical (eupyrene) spermato-
zoa were seen in them, as alsoindicated
by Woodard (1934, 1935) for Goniobasis
laqueata and by Jewell (1931) for G.
livescens correcta, although she did not
13Terminology of Woodard (1935, 1940) and
Magruder (1935b); however, also used. the
term oligopyrene for atypical sperm.
mention the presence of both kinds of
spermatozoa. She observed that the
sperm has a distinctive form, the cylin-
drical head bearing a hook-shaped
structure. Similarly, Magruder (1935b)
reported that the typical sperm of
Pleurocera canaliculatum undulatum
posess a hook-shaped structure whichis
as long as the head. The author
did not observe any such structure
in stained and fresh preparations of
sperm from both P. acuta and G.
livescens.
Female Reproductive System
In many respects, the general mor-
phology of the female reproductive
system is similar to that of the male
(Text Fig. 9). The following organs
compose the system: ovary and oviduct
in the closed tract and lateral and
medial laminae, seminal receptacle, and
nidamental gland in the open tract.
(1) The ovary, which is red to dark
brown, occupies the same position as
the testis in the male.
(2) The oviduct bear the same relation
to the ovary as the sperm duct does to
the testis. It follows a similar course
and, at the level of the stomach, turns
and passes into the body wall. There
is, however, no auxiliary structure
corresponding to the cytophore in this
part of the oviduct. Just before its end,
it makes an abrupt U-turn.
(3) It then is continued by 2 laminae
forming the ‘‘open’’ tract, which corres-
ponds to that in the male, and also
communicates freely with the mantle
cavity. The posterior portion of both the
lateral (right) and medial (left) lamina
are greatly folded. Seenfrom the mantle
cavity these overlapping folds appear as
a swollen sac. The inner walls of these
folds are lined with epithelial cells into
which the spermatozoa, that have entered
the female tract, insert their heads and
remain embedded for an indefinite time.
This sac, therefore, corresponds to the
seminal receptacle of other proso-
branchs. It is probable that it acts as
a reservoir for spermatozoa during the
PLEUROCERA AND GONIOBASIS 39
digestive gland
sperm duct
testis
seminal receptacle
cytophore organ
SE, I prostate
nidamental gland
spermatophore organ
ur lateral lamina
lateral lamina
medial lamina
medial lamina
ne RER NO
anus
27 anus
) osphradium osphradium elle \
o: gills =
E mantle
PLATE IV. Sperm of Goniobasis livescens.
FIG. 1. Typical, eupyrene spermatozoon, similar to that of Goniobasis laqueata illustrated by
Woodard (1935).
FIG. 2. Upper portion of a mature apyrene (atypical) spermatozoon drawn from a fresh smear
preparation.
FIG. 3. Crescent-shaped spermatophore with its tapering ends.
40 B. C. DAZO
entire breeding season.
(4) In the female, the lateral lamina
is thin and narrow but the mediallamina
is swollen and glandular. This gland is
whitish and probably corresponds to the
nidamental gland of other prosobranch
snails. It occupies the region between
the rectum and the genital groove and
extends from the mantle margin to the
posterior surface of the seminal
receptaele over which it is folded. The
nidamental gland is divided into 2 parts,
a shorter anterior or lower more gland-
ular portion and an upper or posterior
less glandular end. The upper portion
is supposedly albumen-producing and the
lower portion may function as a capsule
gland. The entire gland is provided
with numerous ducts which open into the
open channel between the 2 laminae. This
part of the open genital tract seems to
be the counterpart of the pallial oviduct
in other closely allied amnicolid or
hydrobiid prosobranchs such as Pomati-
opsis and Oncomelania.
The fertilization of the egg has not
been studied. It may take place in the
posterior portion of the laminae so
that, as the ova continue through the
open female genital tract, the albumen
and the egg capsule material are added
after fertilization.
According to my observations, the
eggs leave the mantle cavity and reach
the exterior along a channel formed by
the egg-laying groove on the foot and by
the mantle. The eggs remain in the pit
for a brief period, after which they are
pasted to the substrate and finally
covered, either with mud or with sand
grains, in the case of G. livescens or P.
acuta respectively.
Details on eggs and egg-output are
given under life history (p 137-146).
Woodard (1934, 1935) and Magruder
(1935b) gave an excellent description
of the histology of the reproductive
systems of Goniobasis laqueata and
Реитосета canaliculatum undulatum,
which are corroborated by my ob-
servations on P. acuta and G. live-
scens.
median longitudinal muscle
columellar muscle
FIG. 10. The muscular system of Goniobasis
livescens (simplified). Only the main muscu-
lature of the body is given; the columellar
muscle has been somewhat exaggerated to
clarify its location.
Muscular System
Only the 3 major muscle complexes
are considered here: the columellar,
which is the largest and most con-
Spicuous, the pedal and the pharyngeo-
buccal (Text Fig. 10).
(1) The columellar muscle is a broad
and rather flat muscle which attaches the
animal to its heavy shell, and also
serves to retract the operculum, head
and foot. It is attached to the shell
at the side or base of the columella at
the third whorl, always allowing the
animal free play in the penultimate and
body whorls. Its ramifications insert
at various points of the animal, from
the operculum to the head and foot and
the visceral regions.
The median longitudinal muscle in
this complex arises from the mid-dorsal
part of the columellar muscle, at a point
near the bucco-pharyngeal region. This
broad and flat muscle extends forward,
giving rise to 3 pairs of branches: a)
the slender and flat buccal muscles
which branch off from the sides of the
median longitudinal muscle and are in-
serted on the sides of the buccal mass;
b) the muscles which branch off from
the lateral median side of the buccal
mass and insert into the dorso-lateral
part of the head region near the point
PLEUROCERA AND GONIOBASIS 41
where the tentacular nerve innervates the
muscles of the tentacle. These muscles
serve to retract the buccal mass or
lingual organs and the proboscis; c) the
third pair, which arises from the median
longitudinal muscles represents the re-
maining muscles in the proboscis. They
are attached to the ventral wall of the
proboscis just behind the mouth and
below the buccopharynx and serve to
retract the proboscis.
After giving rise to a branch going to
the operculum the columellar muscle
sends off a branch to the foot. It also
sends branches to the sides of the head
which are almost inconspicuous and
form part of the wall of the head and
give rise in turn to smaller muscles
that retract the tentacles.
(2) The foot is made up of a network
of transverse, oblique, circular, and
longitudinal muscle fibers which are
interlaced in all directions to form the
floor of the foot musculature.
(3) The muscular coat of the buccal
mass together with the circular and
longitudinal muscle fibers around the
pharynx form another intricate muscular
system. Connective tissue bands can be
seen crossing below the muscles
retracting the radula, the proboscis, and
the buccal mass. At the same time
the bands connect the lateral walls of the
head region and serve to hold the an-
terior part of the esophagus in place.
ECOLOGICAL STUDIES
Ecological and limnological data were
obtained during the monthly visits to the
4 permanent collecting stations and at
various other collecting sites mainly in
Michigan, positive for P. acuta and G.
livescens.
Three visits were made to the
Tennessee River Valley (Cumberland
Region) where large scale water
impoundment has already caused great
ecological changes and destroyed many
endemic species of mollusks, Thisarea
is probably still the richest in pleuro-
cerids in the North American continent,
More than 300 sites were surveyed out
of which about 200 were positive for
pleurocerid snails (see p 35 and Table
6). Some of these sites willbe described
in detail. A list of the vegetation found
on the shores of, and in the collection
sites, correlating the common and
scientific names of the plants mentioned
in the descriptions, will be found in
Table 1 (p 45).
From my own observations and from
the literature (Woodard (1934), Dawley
(1917), and Goodrich (1945), it appears
that all pleurocerids require clean water.
Р. асща and other species belonging to
the genus Pleurocera prefer to inhabit
relatively larger bodies of water as do
most pleurocerids, except Goniobasis.
Pleurocerids are usually foundin shallow
water, only afewinches deep, though they
may also be found at depths up to 3 feet.
P. acuta snails occupy quiet and sheltered
areas. Generally, they can be regarded
as bottom dwellers since they like to
burrow under the sand most of the time.
They may also burrow under layers of
decaying leaves and other organic
material. С. livescens on the other
hand live in extremely varied habitats,
from natural springs to swift flowing
rivers and open lakes.14 They are often
found clinging or crawling on the sides
of rocks and stones although in lake
situations they, like P. acuta, also burrow
under the sand bottom. The stones
frequented by Goniobasis, are often
densely covered with algae and diatoms.
These habitat selections seemed to in-
dicate that P. acuta is more ofa detritus
feeder. A discussion of food andfeeding
habits is given in a later section (p
64).
Description of Habitats
The Four Permanent Collecting Sta-
tions in Michigan. G.livescens was
144 comprehensive discussion on the habitats
of С. livescens was given by Goodrich
(1945), who also compiled information from
other authors.
42 B. C. DAZO
present in all of these stations, but P.
acuta only in one, the Portage Creek
station.
(1) The Huron River Station at Dexter
This station located at the northeastern
part of the village of Dexter, Washtenaw
County, represents the terminal quarter
mile of Mill Creek, a tributary to the
Huron River; the stream is approxi-
mately 2 miles long and about 25 feet
wide. .In this region, the stream is
well shaded by trees, such as red maple
(compare with Table 1), American white
birch, scarlet oak and rock elm. Some
shrubs, such as gooseberries, winged
sumacs and red-osier dogwoods are
found on the northern bank of the stream
near the collecting site. The stream
bottom contains gravel, stones, oc-
casional sandy-muddy areas where
patches of emergent aquatic plants,
mainly water cress, arrow-heads and
the submerged tape grass are present.
The rocks are usually covered with a
thick algal growth largely composed of
red algae, during the summer and fall.
The water level was observed to
fluctuate a great deal especially in the
course of seasonal changes. In the
spring, when the snow and ice are
melting and when the water level
reached its peak it was almost impossible
to collect snails, for the current was
swift and very strong. Conditions re-
mained turbid and muddy throughout
spring and the summer and fall were
best for collecting. During the winter,
the stream froze over completely; the
animals were then seen lodged under-
neath rocks and stones which tended to
produce air spaces between themandthe
ice cover.
Goniobasis livescens was the most
plentiful mollusk at this station, though
it had a rather spotty distribution. As-
sociated mollusks were the limpet
Laevapex fuscus, the snails Helisoma
anceps, H.trivolvis, Physa gyrina. P.
integra, and the mussel Micromya iris.
(2) The Portage Creek Station. This
collecting site is located at the boundary
line of Washtenaw and Livingston
Counties, on Toma Road. It is approxi-
mately 2 miles north of the University
Radar Observation station and about 3
miles directly south of Pinckney. It
is a relatively small stream, about 4
miles long, originating from Hi-land
Lake in Dexter Township which empties
into Little Portage Lake. It is about 25
to 30 feet wide and, during the summer
and fall months, it has an average depth
of 2 to 3 feet. Although the area freezes
over partially during the winter there is
a continual current at the bottom through-
out the year. In the spring the area is
always flooded and muddy, as is that
near other streams in this vicinity.
This creek is also well shaded by
trees and shrubs. Some ofthe additional
plants noted were: white oak, pin oak,
blackjack oak, mockernut hickory, red
pine, Swamp cottonwood, summer
grapes, poison sumacs and an abundant
growth of poison ivy.
The bottom of this stream has gravel,
rocks and _ stones with many sandy
patches, especially near the sides of the
stream where the banks cut the slopes
rather abruptly. The common emergent
aquatic plants growing there were the
sedges, cut-grasses, arrow-heads and
water cress; among the submerged
vegetation, tape grass, water weeds and
pondweeds were noted.
This station was the only one of the 4
collecting sites where both Pleurocera
acuta and Goniobasis livescens occurred
together. However, closer examination
showed that these 2 pleurocerids tended
to occupy separate and distinct nichesin
this stream, P. acuta being located in
the sandy patches and those with decaying
organic material and С. livescens among
the rocks that were covered with algae.
At this station the most abundant
species of mollusks were P. acuta and
G. livescens; freshwater mussels were
equally plentiful, especially Micromya
ivis, Dysnomia triquetra, Elliptio
dilatatus, Strophitus rigosus, Anodonta
grandis, and Lampsilis siliquoidea.
Other snails present were Campeloma
decisum, Аттсоа limosa, Physa
PLEUROCERA AND GONIOBASIS 43
integra and P. gyrina.
(3) The Kalamazoo River Station.
This site is located near Reiger Park
in the city of Albion, Calhoun County.
The river here is about 20 to 25 feet
wide with an average depth of 2 feet
during the summer and fall. About 500
yards above the collecting site, the river
has been diverted into 3 channels. Dams
were built in 2 of these branches to
produce electrical power while the third
serves as a diversion channel or an out-
let for excess water.
The Kalamazoo River is one of the
longer streams in southwestern Michigan
extending across half the lower Pen-
insula. It has 2 separate headwater
branches, joining just above the city
limits of Albion. The main river flows
through the city and continues to Lake
Michigan as a winding stream.
At the collecting site many trees line
the banks of the river; among them
were: a few scarlet oak, white oak,
swamp cottonwood, American white birch
and many red maples. Patches of cat-
tails and bullrushes grow near the lake
formed by the overflow from the dams.
_ The bottom of this river is very rocky
but has occasional sandy areas. Sub-
merged aquatic plants such as tape
grasses, water weeds, pondweeds, and
stoneworts grow luxuriously in the col-
lecting area. The water flows swiftly
throughout the year and during the winter
months, this stream freezes only along
the sides.
Goniobasis livescens occurred on
rocks, among the water plants andonthe
Sides of the concrete wall of the dam
site. Associated mollusks were: the
snails Physa gyrina, Helisoma trivolvis,
Campeloma decisum; the fresh-water
limpet Laevapex fuscus; andthe mussels
Lampsilis siliquoidea, Micromya iris
and Elliptio dilatatus. Because of the
tremendous amount of pollution from
the city, no mollusks were found down-
stream.
(4) The Zuckey Lake Inlet Station.
This station is located at Lakeland,
Livingston County, Michigan. The
stream, approximately a quarter mile
long and about 4-5 feet wide connects
Island Lake to Zuckey Lake. In its
upper two-thirds this stream has a higher
water level and is surrounded by a
marshy area with an abundant growth of
cattails and arrowhead; the bottom is
muddy and devoid of submerged
vegetation. Along the bank are patches
of red-osier dogwoods but no trees.
Mollusks were found only in the lower
third of the stream.
G. livescens were extremely abundant
and quite evenly distributed over the col-
lecting area. The shells of the adult
Snails were generally smaller than those
from the 3 other stations and most of
them retained their carinae in the nuclear
whorls unlike the other specimens, which
were larger and had smooth whorls. It
was noticeable also that G. livescens at
this station were very black and were
often covered with marl. They were
found on the rocky bottom which was
thickly covered with aquatic plants such
as stoneworts, muskgrasses, arrow-
heads, pondweeds and yellow and white
water lilies. The larger stones and rocks
were often covered with patches of fila-
mentous green and with red algae.
At the collecting site the water had a
depth of about 2 feet or more during
spring, but only 4 to 6 inches during
summer and fall. Other mollusks found
at this site were the snails: Amnicola
limosa, Physa gyrina, and the mussels
Lambsilis siliquoidea, Micromya iris,
and Strophitus rugosus.
Some other habitats in Michigan.
Pleurocera acuta
(1) In western Michigan, an excellent
population of Pleurocera acutawas found
inhabiting the outlet of Big Pigeon River
at Lake Shore Drive, Port Sheldon,
Ottawa County. This station was wide
and lake-like and the current was hardly
noticeable. The depth varied from 1 to
several feet and the bottom was sandy-
muddy. It supported a dense growth of
submerged aquatic plants, such as
44 B. C. DAZO
various species ofpondweeds, stonewort,
water weeds, hornwort and water milfoil.
At the edge of the river there was a
marshy area with cattails, arrow heads
and water lilies. P. acuta was very
abundant in the river outlet where they
were collected among the water plants
and on the sandy bottom. The shells of
these specimens of P. acuta are the
largest in my collection.
(2) Two living P. acuta were collected
in the Huron River at the Zeeb Road
bridge in Scio Township, Washtenaw
County in southeastern Michigan. The
specimens were found crawling on the
sandy bottom in the vicinity ofpatches of
hornwort. Attempts to find these snails
in other parts ofthe river were unsucces-
ful, although previous collectors, such
as Walker and Beecher (1876) and Good-
rich (1943), reported colonies inhabiting
the quiet waters of this stream.
(3) The colony of P. acuta nearest
to the University Museum laboratory was
the one at Honey Creek, Scio Township,
Washtenaw County. Although both P.
acuta and G. livescens live in this small
stream, they are rather sparse there.
The stream, which originates as the
effluent from a group of lakes called the
Sister Lakes, is about 2 miles long and
located within the Ann Arbor city area.
During the summer, the water is only a
few inches deep, exposing much of the
rocks, gravel and sandy patches that
form the stream bottom. Blue-green
and filamentous green algae are abun-
dant. This station does not appear to be
a normal habitat for P. acuta which usu-
ally occurs in relatively large streams.
Goniobasis livescens
In 3 streams in southeastern Michigan
(1, 2, 3 below), in which P. acuta was
previously reported, they can no longer
be found. These streams were, however,
positive for G. livescens. These and
other habitats were:
(1) The Huron River near the outlet
from Portage Lake in Washtenaw
County.
(2) The Kalamazoo River in Calhoun
County.
(3) The Raisin River in Monroe
County.
(4) Two collections of G. livescens
were made, in depths up to 5 feet in
Douglas Lake, Cheboygan County, north-
ern Michigan, where, according to H.B.
Baker (1912, 1942) these snails were
introduced and where they have been a
thriving colony up to the present. One
lot was taken at Grapevine Point, at the
sheltered western shore of the lower
end of the lake, on sandy bottom where
patches of submerged aquatic plants,
consisting mostly of hornwort and water
milfoil grow luxuriously. The other
collection was made at the Sedge Point
area, where the bottom was covered with
mud and marl and had a very thick
growth of stoneworts and muskgrass.
The shells here were covered with
marl, thick and massive, in contrast
to river specimens, whose shells are
much smaller, thin and less bulbous.
(5) A collection of G. livescens was
also made from the north end of the
eastern shore of Burt Lake, Cheboygan
County, northern Michigan. This area
is very much exposed to wind and wave
action. The snails were found crawling
on, or buried in, the sandy bottom and
sometimes they were seen hiding under-
neath decaying driftwood and other vege-
tative matter in the shallow portion of
the lake.
(6) Another batch of G. livescens was
taken from the north part of the western
shore of Silver Beach, Mullet Lake,
Cheboygan County, where the habitat is
very Similar to the one at Burt Lake,
i.e., open to wind and wave action and
devoid of any submerged aquatic plants.
Collecting site in Ohio. Goniobasis
livescens was collected in Lake Erie,
at the Put-in-Bay Biological Station,
in front of the Fishery Hatchery building.
The snails were clinging to the rocks
and gravel near the sheltered shore
and in water about 2 to 3 feet deep.
The shells were a pale yellow-brown,
thick, massive and covered with marl
and red algae.
PLEUROCERA AND GONIOBASIS 45
TABLE 1. Vegetation near and in pleurocerid habitats in Michigan
Common name Latin name
Shade plants common on banks:
Trees
american white birch Betula papyrifera
blackjack oak Quercus marilandia
mockernut hickory Carya tomentosa
pin oak Quercus palustris
red maple Acer rubrum
red pine Pinus resinosa
rock elm Ulmus thomasi
scarlet oak Quercus coccinea
swamp cottonwood Populus heterophylla
white oak Quercus alba
Shrubs
gooseberry Ribes missouriense
poison sumac Rhus vernix
red-osier dogwood Cornus stolonifera
winged sumac Rhus copallina
Other
poison ivy Rhus radicans
summer grape Vites aestivalis
Aquatic plants:
e
emergent
arrow-head Sagittaria latifolia
bullrush Scirpus americanus
cattail Typha latifolia
cut-grass Leersia sp.
sedge Carex sp.
watercress Nasturtium officinale
water lily, yellow Nuphar variegatum
water lily, white Nymphaea odorata
submerged
Algae: - blue green Anabaena sp.
- filamentous green Spirogyra sp.
- redl5 Batrachospermum vagum
muskgrass Nitella flexilis
stonewort Chara vulgaris
hornwort Ceratophyllum demersum
pondweed Potamogeton natans
P. praelongus
P. richardsonii
tape-grass Vallisneria americana
water milfoil Myriophyllum tenellum
water weed Elodea canadensis
15 These were plentiful at many sites in Michigan and also in the Cumberland region (Virginia
and Tenessee) of the southeastern United States.
46 B. C. DAZO
Vegetation.
See Table 1, page 45.
Limnological Data
The limnological procedures followed
have already been indicated under ma-
terials and techniques. Results, in-
cluding data on depth of water and
current, water analysis, temperatures,
and average snail densities from each
of the 4 permanent collecting stations
are given in tabular form in Tables
2, 3, 4 and 5. Corresponding data,
gathered from other positive sites are
shown in Table 6 and for 2 negative
sites in Table 7. RP
Water Levels and Velocities. From
the tabulated data it is evident that the
water levels at the regular collecting
stations, excepting the Kalamazoo River
whose flow is controlled by dams,
reached a peak during the late winter
and spring months (14-38 inches) while
the lowest levels occured in the fall
(3-9 inches). The melting ice and snow
usually causes flooding at the stations,
especially early in spring and also
results in greater flow and higher
velocity readings. The velocities
measured ranged from 0.5-2 feet per
second. .
Water Chemistry. (1) The hydrogen-
ion concentration of the water in posi-
tive areas ranged from 7.5 to 8.6 (that
of the 4 local stations from 7.8 - 8.5).
Shoup and Peyton (1940) and Shoup (1943)
reported that Goniobasis emeryensis was
found in a stream with a pH of 6.2,
which is quite unusual, because pleuro-
cerids are seldom found when the pH
falls below 7.0. Goodrich (1940a), quoting
Shoup et al. (1941), reported that a
branch of the Obey River, whose pH was
above 7.0 in 1939 was “extensively
colonized by these mollusks; [whereas]
in another fork of the river where the
average pH was 6.1 and the lowest was
only 2.6, the area was devoid of any
pleurocerids.’’ In the laboratory,
P. acuta and G. livescens were kept in
containers with a hydrogen-ion con-
centration range from 7.2 (the pH of the
distilled water used) to 8.8, but in tanks
with water of a pH lower than 7.8 they
survived only about 7 weeks and in
containers with a pH higher than 8.5
only 6 weeks. The ideal pH range for
these snails seems to fall between 8.0
and 8.4, at which range all cultures were
ultimately kept in the laboratory. A low
pH, or acidity, is frequently blamed for
shell corrosion in mollusks (see influence
of environmental factors, р 51.
(2) Carbon dioxide is readily soluble
in water to form carbonic acid. How-
ever, some of it is normally carried in
streams as free carbon dioxide. The
metabolic processes of plants and ani-
mals involves the uptake of oxygen and
the production of an appreciable amount
of carbon dioxide. Oxidation brought
about by certain bacteria (Ruttner, 1953)
in the bottom mud or substrate also
accounts for variable amounts of carbon
dioxide. Under ordinary conditions,
water flow and turbulence at rapids and
riffles are sufficient for eliminating
excess carbon dioxide (Shoup, 1950).
However, occasionally the oxygen supply
diminishes and the carbon dioxide con-
tent of the water may rise to a point
detrimental to many fishes and other
biological forms. The behavior of carbon
dioxide is quite different from that of
oxygen and its ecology is not yet well
known. It is, therefore, difficult to make
general statements as to its role as a
limiting factor (Odum, 1959). Shoup
(1950) shared this opinion and mentioned
that there appeared to be but little
accurate information on the true and
exact toxic action of carbon dioxide upon
aquatic organisms.
The amounts of carbon dioxide
recorded in this study were rather low,
i.e. between O and 15 ppm (See Tables
2-6). Whether these small quantities
are a good indication for the presence
of pleurocerids in all the places visited
is unknown.
PLEUROCERA AND GONIOBASIS 47
(3) Total alkalinity was determined by
using methyl orange as an indicator and
was high (about 110-230 ppm). Evi-
dently pleurocerids, especially P. acuta
and G. livescens tolerate (or require)
high alkalinity. These data are similar
to those reported by van der Schalie
(1938), who obtained an alkalinity range
between 133 and 233 ppm in the Huron
River, in Fleming Creek, and in Little
Portage River, a tributary of the Huron
River, streams that have been and still
are positive for G. livescens. Data
obtained by the Institute of Fisheries
Research (Goodrich 1945) also showed
this same high alkalinity for the following
places, all positive for pleurocerids:
Crystal Lake, Benzie County, 111-120
ppm; Muskegon Lake, Muskegon County,
132 ppm; Van Ettan Lake, Iosco County,
136-148 ppm; Big Platte Lake, Benzie
County, 141-156 ppm; Round Lake,
Benzie County, 139-150 ppm; and Mus-
kegon River, Clare County, 87-89 ppm.
Shoup (1943), studying the distribution
of fresh-water gastropods in relation to
total alkalinity, reported that the range
of alkalinity for 25 species of pleuro-
cerids was between 5 and 220 ppm. His
data reveal that these snails tolerate a
wide range of total alkalinity. Shoup,
however, also found that the more
alkaline streams tend to be more pro-
ductive in gastropods, while those with
only 2-6 ppm bicarbonate were very
unproductive since they contained little
or no calcium for shell building.
(4) Pleurocerids are known to require
a fairly good supply of oxygen. This
oxygen need is borne out by the high
amount of dissolved oxygen recorded in
the course of this study. The lowest
reading was 17.63 ppm, taken in Portage
Creek; the highest was 53.86 ppm, at
the Zuckey Lake Inlet.
Prescott (1939) and Goodrich (1945)
observed that a massive destruction of
pleurocerids was brought about by the
depletion of oxygen in lakes by a pro-
longed winter ice cover.
For fresh-water fishes, the minimum
levels of dissolved oxygen were given
as 3-4 ppm by Needham (1938) and as
5 ppm by Ellis (1937). As regards
pleurocerids, the lower limits of
tolerance variously quoted in the liter-
ature are 6 ppm (Shoup and Peyton,
1940), 4.3 ppm for P. acuta (Wiebe,
1928) and 7.8 ppm for pleurocerid life
in general (Jewell, 1920). But, according
to my observations, flourishing colonies
of these sensitive snails seem to be
associated with 20 ppm of oxygen at
least. Beck (1954) considered Gonio-
basis to be among the more sensitive
forms in that they tolerate no appreciable
amount of pollution. Polluted waters
seldom have sufficient oxygen content and
are usually barren of most life forms.
Ortmann (1909), Adams (1915), van der
Schalie (1945), and Goodrich (1945)
attributed the disappearance of pleuro-
cerids and many other aquatic mollusks
to a wide variety of man-made sources
of pollution brought about by “progress”
and by modern industrialization.
Temperature tolerances. In this study
G. livescens was found to tolerate
temperature extremes varying from
freezing up to 80° F. The maximum
temperature measured in the only P.
acuta habitat under regular observation
(Portage Creek Station) was 76° F. At
the Huron River Station G. livescens
was found to survive under the ice with
tightly closed apertures, hidden under-
neath stones or under layers of decaying
organic matter in the manner already
described by Goodrich (1945) in un-
frozen streams (See Seasonal activities,
р 63). During the hot summer months
when the water is only a few inches
deep they did not seem disturbed by
the direct rays of the sun. Regarding
heat tolerance, a laboratory experiment
was conducted by Nash (1954) to deter-
mine the temperature and exposure time
necessary to cause death by heat in G.
livescens. She established that the
critical temperature that wouldkillafter
one hour's exposure was 36° С (96.89Е);
that, if the temperature was below 369C
B. C. DAZO
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PLEUROCERA AND GONIOBASIS
51
TABLE 7. Limnological data from two sites negative for pleurocerids at Oakridge, Теппеззее19
Average
Depth of
Water
(inches)
Temperature
Locality
East Fork
Branch Poplar
Creek
Creek #64
Hydrogen-
ion Conc-
entration
(pH)
Free Dissolved Methyl
Carbon Oxygen Orange
Dioxide Content Alkalinity
(ppm) (ppm) (ppm)
147.0
19The above data appear to lie within the limits of toleranceand do not explain the absence of
pleurocerids.
these snails could tolerate longer ex-
posures and if it was above 360 С,
they tolerated only short exposure
times.
Snail densities. The procedure fol-
lowed in determining snail densities at
the permanent collecting stations has
been described under sampling methods
(p 11-12). The average densities,
for each visit, are given in Tables 2, 3,
4 and 5. For localities other than the
regular stations (Table 6), the average
snail density refers to all of the pleuro-
cerid snails inhabiting the area and the
number of snails is only an approxi-
mation.
Among the 4 permanent stations, the
Zuckey Lake Inlet station was the richest
in G. livescens, with a maximum of 892
snails per square meter area in Sep-
tember 1960 and an average of 531.
The Portage Creek station had the
lowest density, with a corresponding
average of only about 38 snails while
at the same station P. acuta, was even
less numerous, with an average of 24.
The limited data available do not allow
interpretation in terms of population
dynamics. However, the highest records
for snail densities in all 4 permanent
stations were obtained during summer
and fall.
Influence of Environmental Factors on
Shell.
Among the Pleuroceridae, as in many
other molluscan groups, both intra-
and interspecific variation is common,
and in consequence, the taxonomy ofthis
group also remains in a very confused
state. The extent of shell variation of
the species called Goniobasis livescens
since Goodrich’s (1945) comprehensive
study, is well illustrated by the fact that
various authors in the past have believed
it to belong to several different species;
Walker (1893), originally used 8 names.
However, Goodrich (1945) surmised that
there were certain basic and constant
characters in the internal anatomy of
G. livescens to indicate that all of the
forms in Michigan represent but one
polymorphic species. My observations,
based on specimens collected from vari-
ous localities in Michigan clearly support
this view (Fig. 11 and Table 13).
There is evidence that shell, form in
mollusks may be influenced by environ-
mental factors, such as wave action,
current, substratum, etc. For the
Pleuroceridae, one of the earliest ob-
servations was made by Bartsch (1906)
on variations in Goniobasis virginica of
the Potomac River, but he did not
correlate them with environmental con-
ditions. Adams (1900, 1915) intensively
studied the pleurocerid genus Jo in
Tennessee and clearly showed the
occurrence of geographical variation,
which corresponds to a clinal variation
in the course of a river system. He
attributed the variation, in part, to
52 B. C. DAZO
9 10
FIG 11.
A. Goniobasis livescens
ea
13 14
Shell variation in Goniobasis livescens and Pleurocera acuta fromvarious localities.
1. 1-year old, laboratory bred. Note single carina on whorls.
2. 2-year old, laboratory bred. Note single carina on whorls.
3. Zuckey Lake Inlet Station, Livingston Co. , Michigan.
4. Portage Creek Station, Livingston-Washtenaw Co. Line, Michigan.
5. Kalamazoo River Station, Calhoun Co. , Michigan
6. Huron River Station, Washtenaw Co. , Michigan.
7. Shore of Lake Erie (U. S. Fishery Hatchery Station), Put-in-Bay, Ohio.
8. Grapevine Point, Douglas Lake, Cheboygan Co. , Michigan.
B. Pleurocera acuta
9. 1-year old, laboratory bred. Note double carinae in whorls.
10. 2-year old, laboratory bred. Note double carinae in last whorls.
11. Portage Creek Station, Livingston-Washtenaw Co. Line, Michigan.
12. Huron River near Zeeb Road bridge, Scio Township, Washtenaw Co. , Michigan.
13. Honey Creek, Scio Township, Washtenaw Co. , Michigan.
14. Big Pigeon River at Lake Shore Drive, Port Sheldon, Ottawa Co. , Michigan.
chemical differences, stating “That there
are chemical differences in the differ-
ent parts of the river, and further
that these influences affect these snails
., that the shells do not abound in
waters other than those draining lime-
bearing rocks, clearly shows that lime
is a limiting factor in their range.”
He realized, however, that chemical fac-
tors do not suffice to explain variation:
“From the standpoint of chemical com-
position of the water the presence of
mixed communities of shells as near
Rogersville, with great extremes from
smooth to spinose shell on the same
shoal, is particularly confusing, because
we cannot believe that in such a situ-
ation the agitated waters can show a
corresponding chemical diversifica-
tion.”
The occurrence and variable extent
of erosion in Goniobasis was noted by
PLEUROCERA AND GONIOBASIS 53
Clench (1926). Since it occurred in
locations where the mechanical action
of waves or current were not the caus-
ative factors, he attributed it to chem-
ical action. Reports on the corrosion
of snail shells are common; it is usually
attributed to the action of acid water
or sometimes also to abrasion by other
snails in quest of lime. Goodrich
(1940a) attributed irregularities in the
suture and corrosion of the shell, such
that all of the epidermis was removed
except on the body whorl or part of
it, to the direct effect of low pH.
Frómming (1956), however, points out
that such corrosions may be present
in lime-bearing waters and absent in
waters rich in carbon dioxide and humic
acids, that frequently not all specimens
of a colony are corroded and that both
corroded and uncorroded colonies may
occur in one and the same lake. He
supports the idea that the periostracum
of the snails must first be damaged
by certain algae, before corrosion can
take place. The writer has observed
pleurocerid colonies in a stream at
Oak Ridge, Tennessee, containing
pleurocerids only, where every single
snail, young or adult, showed advanced
corrosion.
Baily, Pearl and Winsor (1932, 1933a,
1933b) studied variations in Goniobasis
virginica and Anculosa carinata under
natural conditions. They concluded that
the variation in the size of the shell
was influenced by chlorine, food supply,
silt, and other environmental factors.
Wiebe (1926) studied variations of
G. livescens in several stations in Lake
Erie. He showed that the average shell
obesity, i.e., the ratio of shell diame-
ter to total length, was directly pro-
portional to the degree of exposure to
wave action. The snails subjected to
almost continuous wave action had more
bulbous or obese shells, while those
that inhabit more sheltered areas pos-
sessed long and slender shells. Wiebe
thought that snails exposed to wave ac-
tion probably develop so slowly that
the shell may never develop its full
number of whorls or that the direction
of growth may be altered altogether;
consequently, such shells become short
and obese rather than long and slender.
A similar increased obesity with wave
action is reported by Boettger (1944)
for Lymnaea spp.
An interesting laboratory experiment
by Plaget (1929) has a bearing on shell
form in relation to exposure. He had
found that in exposed situations in lakes,
the shells of Lymnaea siagnalis had
relatively short spires and long aper-
tures. When these snails were raised
in laboratory tanks, the offspring pro-
duced longer spires than their progeni-
tors. When these long spired forms
were raised in a mechanically agitated
aquarium, the young produced even
shorter spires and longer aperturesthan
their wild grandparents.
Cheatum and Mouzon (1934) used bio-
metry in their study of Goniobasis
comalensis Pilsbry. They found that,
on the average, pond dwellers had greater
length and diameter than the river forms.
They also showed that the mean ratio
of diameter to length of the shells among
river forms was greater than that for
pond specimens. Goodrich (1945) re-
ported that loose coiling was more
characteristic of Goniobasis in sheltered
situations; tight coiling was more pre-
valent among snails in western Lake
Erie in the more open habitats.
F. C. Baker (1928b), in his Wis-
consin report, recognized 4 forms of
G. livescens, according to the habitat
occupied by the so-called species, as
follows: (1) G. livescens; witha smooth,
acute shell characterized by narrow
whorls, inhabits bays andrivers entering
the Great Lakes; (2) С.1. michigan-
ensis, with a bulbous body whorl, a
wider spire, and a thick shell and lip,
lives on exposed lake shores; (3) G.
l. correcta, a small river form with
a less elongated spire,6-8 whorls, a
narrower, more elongated aperture, and
a rounded bulbous body whorl, is found
in quiet rivers and their pond-like ex-
tensions in Wisconsin; and (4) G. l.
B. C. DAZO
54
PLATE V
PLEUROCERA AND GONIOBASIS 55
barronensis, characterized by its elon-
gated shell with very flat-sided whorls
and raised spiral ridges on the body
whorl, is found in small, swift flowing
rivers.
LIFE HISTORY
As already mentioned, only few ci-
tations dealing with the life history of
pleurocerid snails are found in the
literature.
Mating habits
It is shown below (see p 56-60), (Egg
laying season and potential) that
in Michigan P. acuta and G. livescens
begin to oviposit in April as soon as
they become active in spring, with a
peak of egg laying activities in April
and May, and that, having apparently
exhausted their egg laying potential, P.
acuta will not oviposit after June nor
G. livescens after the middle of August.
Both species, collected in the field
late in the fall and acclimatized in the
laboratory, laid eggs on the sides of
the containers a few days after they
were transferred to thelaboratory. This
sequence of events indicates that mating
must have taken place sometime earlier
in the fall.
It is believed that mating is most
common in the fall, when these snails
are very active in their natural habi-
tats though it is possible that copu-
lation may also take place during spring.
In the laboratory it was very diffi-
cult to observe the mating habits, be-
cause these snails are without external
genitalia. However, they were observed
to assume positions suggesting that they
copulate like other prosobranchs. When
associated individuals were thus sus-
pected of copulating they were immedi-
ately isolated in separate containers.
The presence of spermatophores in the
water was then taken to indicate that
the couple actually did so, and their
absence, that the snails had been
crawling inadvertantly over each other.
That mating actually occurred in the fall
is also borne out by cytological evi-
dence (p 64). Jewell (1931) experienced
the same difficulties in her studies
of! Ga lo correcta. It appears that
the female genital sinus, in addition
to its function of assisting oviposition
by contraction, also functions as
a bursa during copulation. A simi-
lar opinion was also expressed by
Woodard (1934), who stated: “Since
Spermatozoa and spermatophore rem-
nants are frequently found in the sinus,
and since no spermatophores are ever
found intact between the laminae in
females, and hence, must never be in-
troduced there, it must be inferred that
the spermatophores are _ shed by the
males and collected into the sinus by
females.” It would seem that the sperma-
tophores break down as soon as they
reach the genital sinus. The released
Spermatozoa then find their way to the
seminal receptacle by way of the gen-
ital groove and laminae. Woodard (1934)
also suggested that possibly the migra-
tion of sperm takes place only when
the females are retracted in their shells
so that the genital pit, with the shell,
PLATE V.
FIGS. 1& 2. The egg masses of Pleurocera acuta
FIG. 1. Detached egg masses of various shapes; some from the lower side (not coated
with sand). 13X.
FIG. 2. Recently laid egg clutch with embryos in the second cellular division (trans-
mitted light). 30X.
FIGS. 3&4. The eggs of Goniobasis livescens
FIG. 3. The upper egg has the characteristic coating of soil; the lower one was turned
over to show the egg itself. 25X.
FIG. 4. Newly laid egg with its covering of soil. 60X.
56 B. C. DAZO
forms a duct to insure a safer transit
for the immigrating sperm.
The Egg and Egg-Laying Activities
- Eggs and Egg Clutches, The average
diameter of the ovum of P..acuta (from
over 500 measurements) is about 300u
and, with its membrane, about 350 u.
The eggs are encased in clear spherical
compartments, whichare surrounded by
a transparent, gelatinous matrix. In
color the eggs vary from gray tobluish-
green; sometimes they appear light yel-
low, orange or pink. Within the egg
mass or clutch the eggs do not seem
to be arranged in any definite pattern.
A general description of the eggs of
this species as well as of P. lewisii
is given by Van Cleave (1932).
The eggs are deposited in masses
which vary in size (on the average
1.5-2.0 mm) and shape (Plate V, Figs.
1 and 2) and may contain from 1-19
eggs. In side view, each egg mass
has a plano-convex shape, the flat side
adhering to the solid substratum to which
the snail attaches its eggs; the convex
upper side is usually coated with minute
sand grains which the parent snails place
there during the process of egg laying.
Van Cleave (1932) describes the clumped
eggs with their coating as having the
appearance of insect cases.
The egg masses of P. acuta are
deposited on a wide variety of objects,
such as stones, leaves, and discarded
empty beer cans and bottles. It is not
uncommon to find eggs deposited on
the shells of other live specimens.
Jewell (1931) gave a good descrip-
tion of the egg of Goniobasis livescens
correcta (from Illinois): “Eggs always
appeared singly or in lines of two or
three with no covering except the simple
Shell membrane which remained until
the time of hatching. Little variation
was found in the size of the newly laid
eggs. The size most frequently found
was 306 „ as the diameter of the egg
itself within a membrane of 382 u to
425 u in diameter.” The details of
this description also apply to G. live-
scens in Michigan, except for minor dif-
ferences in size. The eggs of the local
G. livescens were smaller, measuring
about 280 „ in diameter; with the egg
membrane, the average diameter was
330 u (from over 300 measurements)
(Plate V, Figs. 3 and 4). Rows for
lines) of 2-3 eggs were likewise noted;
these were about 3 cm apart from one
another. The eggs were quite hard to
see; I first observed them on the sides
of the aquaria in March, 1959 and I
was able to find them only a year later
in the field. These eggs, which are
also laid on solid objects, lack a sand
grain cover, but are coated with a thin
layer of soil and blend perfectly with
their background. If the thin soil coat
is removed, a whitish-gray ovum is
exposed that is surrounded by a clear
gelatinous membrane.
A brief comparison of the spawn of
the 2 snails here described with that
of other pleurocerids may be found in
Table 9, and a discussion of the pos-
sible significance of the various types
on classification, on p 172.
Egg Laying Season and Potential. The
combined information obtained for both
species in the field and in the laboratory
indicates that P. acuta produces eggs
during a shorter period (April-June)
than does G. livescens (April through
mid-August). It should be noted however
that P. acuta has a greater egg laying
rate (per snail per day) than С. live-
scens (15 as compared to 4).
The approximate egg-laying potential
of P. acuta was determined as follows:
45 adult females were collected at the
Portage Creek station on April 20, 1960,
a period when eggs usually begin to
appear in nature. In that instance,
however, the water temperature at the
station was only about 50°F and there
was no egg-laying yet. The snails were
kept at room temperature (72°F). Within
a few days the snails began to deposit
eggs on the sides of the container and
continued to do so over a period of
about 4 weeks, after which no more
eggs were deposited. Throughout the
PLEUROCERA AND GONIOBASIS 97
egg-laying period a daily record was
made of the total number of egg masses
and the number of eggs per mass. Most
of the clutches were laid on the glass
sides of the aquarium. These were
marked witha red wax pencilas they were
laid; the few clutches in other locations
were also recorded. From day to day the
unmarked clutches represented the newly
laid eggs. A total of 2,096 egg masses
with 18864 eggs were laid in 256 days.
Assuming that all 45 snails were gravid,
each female had produced an average
of 46.5 egg masses. With an average
of 9 eggs per mass, it is calculated
that a single female produced a total
of 398.7 eggs, or an average of about
15 eggs per day. However, about 80%
of the eggs were laid during the first
2 weeks of the egg-laying period.
The same procedure was repeated in
2 successive experiments, one beginning
June 20, and the other on July 27, 1960.
The earlier culture only gave positive
results, the snails laying a few eggs,
for one week; this clearly indicates that
in nature egg-laying does not extend
beyond June.
_ It was determined among laboratory
raised P. acuta that the animals ovi-
posited for the first time when they
were about 2 years old. The egg-laying
activities of 2 age groups, one in their
first and the other in their second egg-
laying season, were compared by taking
100 egg masses at random from each
group and counting the number of eggs
(Table 8). It was found that young
adults generally laid fewer eggs per mass
than did the older group, the average
number of eggs per clutch being 2.81
and 6.62 respectively, and that these
laboratory bred snails laid smaller egg
clutches than did those from the field,
with 4.7 eggs per mass against 9.
For possible reasons, see stunted growth
of cultured animals (p 61). Van Cleave
(1932) reported an average of 4-5 eggs
per clutch.
The egg-laying capacity of G. live-
Scens was Similarly studied. Forty adult
females, collected on April 19, 1960,
TABLE 8. Number of eggs per clutch in
laboratory bred Pleurocera acuta
of two different age groups.
Approximate age of snails
2 years 3 years
(beginning of (fully
egg-laying) matured)
4 4 DHL 0:5 5 8 Оо
3 4 STAY oe 4 5 бп 6
5 4 PA 5 9 5 21608
1 2 4 4 6 8 5 6 4 4
Ad AA o 1 2 LME NT
5 3 ASIS 7 4 DOS
1 3 Be 3 Val 5 6 ALIAS
2 2 Sie eS 7 5 By ts al
2 1 de ya te A 6 8 DNS ND
4 3 4 1 4 7 7 Dien
il 2 тыл 7 4 Ci) 7510235
1 3 22.21 14 4 CAOS
4 2 SAS 71.714 nt
5 5 rl 6 4 8 4 6
3 2 4 3 4 5 6 AO AO
3 il SAS 6 5 OI
3 3 PAN A 275716
1 1 SEL 9 1 ZAS
5 i I Au 6 Би AG
5 3 EC 6019 4
Average number of eggs рег clutch
from 100 random clutches:
2.81 6. 62
from the 200 clutches:
4.71
at the Huron River station were main-
tained in the laboratory. Over an ob-
servational period of 20 days, they
produced a total of 3,264 eggs, cor-
responding to a mean of 81.6 eggs per
female, and an average of 4.08 eggs
per day. Two additional series of 40
snails each were observed using snails
collected from the Kalamazoo River and
the Huron River stations, on July 22
and on August 5, 1960. Since all these
snails produced eggs, although fewer in
number, another batch was collected
on August 18, 1960. These failed to
oviposit and it is concluded that eggs
58 B. C. DAZO
TABLE 9. Comparison of egg-laying among twelve species of Pleuroceridae
Species Egg deposition and average
egg output per snail
Pleurocera acuta (Dazo: 1-19 eggs/mass; about 15 eggs/day).
Pleurocera lewisii Eggs in masses sparsely covered with sand;
flat, with gelatinous covering; range 3-15 eggs;
avg. 7-8 eggs per mass; egg-laying time per
mass 45 min.
Eggs in masses with or without a cover of sand
grains or soil; range 3-13 eggs; avg. about 9
eggs per mass; diam. of each mass 1-1.7 mm.
Pleurocera canaliculata
Goniobasis livescens correcta Eggs laid singly, or 2-3 in a row; no sand
cover; shell membrane covering alone.
Eggs laid singly, or 2-3 ша row about 3 cm
apart; covered with thin layer of soil; about 4
eggs per day.
Goniobasis livescens
Eggs laid singly; with thin soil or detritus
covering; no sand grains.
Goniobasis clavaeformis
Eggs in plano-convex egg-mass, 1-1.7 mmin
diam.; sparsely covered with sand; about 4-
16 eggs per capsule.
Data confirmed, Dazo.
Goniobasis laqueata
Eggs in masses with 2-15 eggs or more; eggs
spirally arranged, with fairly tough outer mem-
branous cover forming septa and dividing mass
into compartments; foreign matter attached to
egg mass.
Goniobasis virginica
Eggs laid singly, or 3-6 or more usually in a
row; successive capsules connected bya
thread-like portion of outer egg membrane;
with sand covering.
Anculosa carinata
Lithasia venusta Eggs laid in pairs opposite each other in a con-
tinuous ribbon; diam. of egg mass about linch.
Eggs in ribbon-like gelatinous, transparent
mass devoid of sand covering; a mass meas-
sures on avg. 9.27 by 2.70mm; eggs arranged
diagonally with respect to length of mass in
rows of 1-5 eggs; 182 eggs per day.
Io fluvialis
Anculosa (“Leptoxis”) sp. Eggs laid singly.
Average Diameter
of Egg in Microns
300
285
300
306
275
280
300
(Dazo)
No data
No data
No data
350
700-1000
PLEUROCERA AND GONIOBASIS
TABLE 9 (continued)
Egg-laying Period Development of
and Region Egg in Days
April to June
Illinois
March to April
Illinois
May
Tennessee
March to June
Illinois
April to middle of
August
Michigan
April to June
Tennessee
January to May
Tennessee
June
Maryland
June
Maryland
January to May
Tennessee
April to May
(laboratory,
Ann Arbor, Mich.)
No data
15 - 16
(72° F)
(Dazo)
No data
15
11.5
15
(72° F)
No data
15
(72° F)
(Dazo)
No data
No data
No data
15
(7225)
No data
59
Author and Citation
Van Cleave, 1932
Van Cleave, 1932
Rosewater, 1959
Jewell, 1931
Dazo
New data.
Dazo.
Unpublished data.
Woodard, 1934
Winsor, 1933
Winsor, 1933
Woodard, 1934
Dazo, 1961
Rosewater, 1960b
60 B. C. DAZO
are not deposited in nature beyond the
middle of August.
Data on the eggs, egg clutches, season
of oviposition and length of development
for 12 pleurocerid species belonging to
6 genera, have been compiled in Table
9 from the literature and from personal
observation.
As regards the egg-laying season it
appears that pleurocerids in various
parts of the United States generally
oviposit in spring and early summer,
though in Tennessee 2 species are re-
ported to start as early as January.
My field observations in various streams
of Tennessee and Virginia further in-
dicate that, in these southeastern parts,
there also occurs another reproductive
season in the fall. Van Cleave's findings
(1932, 1933) that P. acuta oviposits from
April to June, in Illinois, are entirely
corroborated, for Michigan, by my own.
The long egg laying season of G. lives-
cens here reported is, however, in con-
trast to the data reported for other
species.
Time of Development in the Egg and
Gross Embryology
Except for some minor details, the
embryonic period of P. acuta and G.
livescens is about the same. At room
temperature (720F), the young hatch
about 2 weeks after oviposition; the
developmental process is the same for
both species. Hence, only one general
outline on the gross embryology isgiven
in Table 10. Although 15 days are
here given as the time for the develop-
ment of the eggs, young may hatch several
days beyond the normal period. Fully
developed snails were often observed
“sitting” within the egg case. Basch
(1959), in his account of the basommato-
phoran fresh-water limpet Ferrissia
shimekii (Pilsbry) reported that the
young were often in no hurry to emerge
and may remain in the egg capsule for
Several weeks without any apparent ill
effects.
The newly hatched P. acuta were, on
the average, 340 y long and 450 y wide;
G. livescens were about 270 u long
and 380 u wide. At that stage the
shells of both species closely resemble
figures given by Jewell (1931) and
Winsor (1933) for other species of Gonio-
basis and Anculosa. Newly hatched
Snails were observed to be quite active;
they moved continuously on the bottom
and sides of the aquaria apparently
serching for their first meal.
Growth
On April 27, 1959 and May 2, 1960,
adult female P. acuta from Portage
Creek station were brought into the
laboratory and on April 30, 1960, speci-
mens of С. livescens from the inlet to
Zuckey Lake. These snails laid eggs
in the indoor tanks a few days after
they were collected. The young ob-
tained were used for growth studies.
The shell of the newly hatched snails
has one whorl, but occasionally there
may be the beginning of a second whorl.
The data given in Tables 11 and 12
represent measurements of laboratory-
raised snails of both sexes. In each
Species 2 batches belonging to 2 different
age groups were measured at intervals.
The first series comprises snails less
than one year old; it started with groups
of about 150 individuals which, however,
declined with each subsequent measure-
ment, till only a few specimens were
left in each case. The second series
comprises snails over one year old and
covers groups declining from 44-17
individuals in the case of P. acuta and
from 300-135 individuals in that of
G. livescens. Since growth studies on
P. acuta had started earlier it was
possible to obtain more data on that
Species. Development was more pro-
nounced during the first year (from an
average length of 0.34-10.8 mm) and
growth then continued slowly even after
sexual maturity (copulation) at 18
months, when they reach 13.95 mm,
to 16.72 mm at 2 years, after which
time no appreciable growth occurs. The
corresponding figures for G. livescens
are 0.27-3.87 mm atone year ofage, 5.15
PLEUROCERA AND GONIOBASIS 61
TABLE 10. General observations on the embryonic development of Pleurocera acuta and
Goniobasis livescens, at 72°F.
Agein
Days
1 Cleavage begins about 2 hours after eggs are laid; development from 4 to 8 cell stage;
extrusion of polar bodies observed.
2 Cell division produces many cells (32 to 64); general shape of egg changes from spherical
to slightly ovoid.
3 Embryos in blastula stage; some rotate slowly, counterclockwise; others remain in multi-
cellular stage.
4 Gastrula stage; more pronounced rutation of embryos; period of organ formation.
5 Trochophore stage; rotation continues.
6 Appearance of velum in some specimens;
continues.
general shape approaches a veliger; rotation
7 Velum more visible; body begins to be organized with respect to position of head, foot and
shell; rotation continues.
8 Velum very prominent; veliger stage reached; rotation slows down.
9 First heartbeat observed in some specimens; foot begins to move; velum remains large.
10 Velum beginning to contract; foot movements and beating of heart more pronounced; ro-
tation ceases.
11 Velum much reduced; foot movements and heartbeats very pronounced.
12 Velum disappears;
young have formed and move actively; eyes visible at swollen outer
base of tentacles; proboscis with lips; shell begins to take shape.
14)
1
3) Fully formed young with shell (one whorl); very active inside capsule.
15 Young begin to hatch, though hatching may be delayed for several days.
mm at sexual maturity and 6.96 mm
at 2 years of age. The data indicate
that the laboratory raised snails (Tables
11 and 12) are much smaller than field
specimens (Table 13) having the same
number of whorls. P. acuta with 9-11
whorls measured about 16.5 mm in the
laboratory and from 26.5-31.5 mm in
the field (i.e. 1 1/2 to twice as much)
and С. livescens with 7 whorls measured
between 6 and 7 mm in the laboratory,
while field specimens with 7-9 whorls
were twice to 3 times that size (13.76-
22.70 mm). This difference (as also
the difference in fertility, see p 144)
may have been due to crowding and per-
haps to a lack of necessary nutrients
in the laboratory tanks. It is also
possible that too much handling of the
animals might have accounted for the
stunted growth of the cultured animals.
Sexual Maturity and Longevity
Definite information on the life span
of the 2 pleurocerid snails under study
has not been published before.
As already indicated, the laboratory
raised snails attain sexual maturity at
the age of 18 months and begin to lay
eggs at the age of 2 years, at which
time the average length of Pleurocera
acuta is about 16.7 mm and its width
6.6 mm; the corresponding average
measurements for Goniobasis livescens
are 7 mm and 4.5 mm. We have also
seen (Table 8) that fewer eggs were
62 B. C. DAZO
TABLE 11. Size of laboratory bred Pleurocera acuta and their corresponding age
Number of
Snails used
Number of
Whorls
Average size in mm
LIPuNNEOSoS
ялревннно?е?
in months
12 5. 44
15 5. 41
18 6. 40
21 6. 37
24 6. 31
27 6. 24
30 6. 20
33 6. 1br
Number of
Snails Used
Number of
Whorls
Average size inmm
0. 0. 1
0. 0. 1.5 132
0. 0. 2 102
0. 0. 3 79
1: if 4 48
its il 4.5 25
2. 2. 5-6 18
3. 2. 5 - 6.5 13
4. 2. D'or
in months
12 300
15 280
18 227
21 162
24
PLEUROCERA AND GONIOBASIS
TABLE 13. Sizes of adult snails collected at
various localities in Michigan
and Ohio
Average size inmm
Pleurocera acuta20
Portage Creek 29.10 11. 28
Big Pigeon River 32.70 12. 91
Honey Creek 26. 62 11.10
Spring Lake 29.70 т
Grand River 31.50 125 Bl
Total: 149. 62 58. 95
Average: 29.92 Tals TE)
Goniobasis
livescens21
Zuckey Lake Inlet 13276 elo
Kalamazoo River 14. 50 7.88
Portage Creek 15.60 8. 00
Huron River 17. 30 8.41
Honey Creek 21. 03 9. 83
Burt Lake 18. 98 9. 92
Douglas Lake 20. 32 8.49
Mullet Lake 20. 45 9. 49
Lake Erie22 22.20 9.45
Total: 164. 14 79. 08
Average: 18.24 8.79
20Number of whorls 9-11; 669 snails used.
21Number of whorls 7-9; 9261 snails used.
220nly locality in Ohio.
laid by P.acuta that had just begun
to oviposit than by the older, fully
matured snails (2.8 eggs per clutch
as compared to 6.2).
The field and laboratory data indicate
that both P. acuta and G. livescens
attain an age of about 3 years. Rose-
water (1960) assumed the same longe-
vity for P. canaliculata. The life span
63
of the 2 species studied here may ex-
tend to 4 years perhaps, depending on
the environmental conditions to which
the colonies are subjected. In open
areas, such as the exposed shores of
inland lakes where the animals are con-
tinuously exposed to windand wave action
during the warmer months and to de-
pletion of oxygen in the winter, it is
hardly conceivable that these snails can
live up to 4 years. On the other hand,
colonies occupying sheltered or more
protected habitats may have a better
chance to live for more than 3 years.
Sex Ratio
Snails of both species from the per-
manent collecting stations and from labo-
ratory cultures were examined as to sex.
It was found that females outnumbered
males both in the field populations and
the laboratory colonies, especially so
in the latter, and especially for G.
livescens, (Table 14), the overall sex
ratios being roughly 2:1 for P. acuta
and 5:1 for G. livescens.
That the laboratory raised specimens
of both species showed a much higher
ratio in favor of the females than those
from the field seems to indicate that
the females tolerate artificial conditions
better than the males.
Diurnal and Seasonal Activities
In nature, G. livescens are often ob-
served crawling over the sides of rocks,
stone and various solid objects, ap-
parently scraping off algae and diatoms
in the process of feeding. Now and
then they pause for a while but usually
the restless hunt for food goes on.
In contrast, P. acuta is somewhat slug-
gish. It slowly plows through the sandy
TABLE 14. Ratios of females to males in adult Pleurocera acuta and Goniobasis livescens
Speci Laboratory
eas bred snails
P. acuta
G. livescens
Field Overall
snails ratio
Dale 130 1.85 74
6.50 2.42 4.71 318
No. of snails used
Lab. bred
64 B. C. DAZO
bottom with its rostrum fully extended.
F. C. Baker (1928a) described its move-
ment as follows: “Its rostrum is like
an elephant’s trunk or a hog’s snout
waving about from side to side, examing
the bottom--this reminds one of a dog
on the scent”... “when progressing,
the animal glides along for a short
distance, then pulls the shell after it,
thus advancing by a succession of jerks.”
In the laboratory, both P. acuta and
G. livescens preferred to stay on the
bottom of the glass aquaria in the
evening. The former species often re-
mained buried halfway in the sand; some
protruded their rostrum partly from the
shell while their tentacles slowly moved
about. G. livescens would simply “sit”
on top of or on the sides of rocks or
gravel with little or none of the head
region visible. As day begins, the
animals of both species again ascend the
sides of the aquaria. Whether this
habit is a direct response to light or
associated with feeding is unknown.
Goodrich (1945) reported that 5°C
was the lowest temperature at which he
observed G. livescens on the upper sides
of stones in the Huron River. When
the temperature had dropped to 1.1°C
he (and Jackowski) noticed that all the
snails had disappeared. They found the
animals hibernating under stones or in
gravel and sand, in water flowing too
fast to freeze. Their apertures were
tightly closed by their opercula; the
Shells were covered with a film of
white material which they assumed to
be gelatinous algae. Goodrich reported
May 1, 1943, as the earliest spring
date at which he saw the snails active.
He realized that the end of hibernation
might have occurred earlier but had
not been discovered because of high
water and the turbidity common during
the flood season. I have usually found
these snails active at an earlier date,
in the second half of April.
Egg laying starts in spring when the
lake and stream waters begin to warm
up. As already discussed, breeding con-
tinues through the early part of summer
(p 56). In view of their increased
activities, summer and fall are the
best times for collecting and studying
pleurocerids. Many snails crowd to-
gether in distinct colonies, and their
distribution in the stream or lake is
somewhat spotty.
The juveniles of both species are often
observed floating at the surface of the
water with their shell hanging down-
ward and the foot adhering to the sur-
face film. On closer examination the
foot was found to assume a cup-like
shape that created a partial vacuum be-
tween it and the thin film of water.
Another pattern of behavior noted was
the habit of these snails to come to
the top of the water, where they ex-
tended their rostrum above the surface.
They would remain in this position for
hours. F. C. Baker (1902) observed
the same in С. livescens.
Michigan pleurocerids are very active
in the fall. At this season they can
frequently be seen taking up the “mating
position.” That laboratory bred snails
lay eggs in midwinter, seems to bear
out previous mating (p55). Further
evidence for fall mating is furnished by
the presence of fertilized eggs in gonad
sections of P. acuta and G. livescens
collected during winter (Plates VI and
УП, Figs. 2 and 3). In nature hiber-
nation begins immediately with the in-
ception of winter conditions and the eggs
are laid in spring only.
Food and Feeding Habits
About 200 P. acuta and 250 G. lives-
cens from the permanent and occasional
stations were used in this study. They
were fixed and preserved in Lavdowsky’s
solution (formalin: alcohol: acetic acid
2:10:1 parts per volume).
In the laboratory the stomach con-
tents were examined microscopically.
Algae, including green and red algae,
diatoms and desmids, were found to
constitute a major part of the diet of
both species, which do not differ in
this respect from Oncomelania quadrasi
snails (Dazo and Moreno, 1962). A
PLEUROCERA AND GONIOBASIS 65
PLATE VI. Histological sections of Pleurocera acuta.
FIG.
FIG.
FIG.
FIG.
FIG.
FIG.
1.
Cross section of the visceral region showing the position of the 2 chambered heart (H),
the much folded structure of the kidney (K), the esophagus (E), the stomach (S), and
the intestine (I).
Cross section of the ovary (O) of a specimen collected in the winter withripe ova in the.
gonad. Note liver (L) pigments in lower left corner. Approx. 200X.
Cross section of the testis (T) of a specimen collected in the fall, showing the charac-
teristically oriented spermatozoa in the gonad. Liver (L) cells with dark stained pig-
ments can be seen in lower half. Approx. 200X.
Longitudinal section of the mantle region showing cross sections of the gill filaments.
The large intestine appears in the lower right corner. ' Approx. 30X.
Longitudinal section of the head-trunk region showing mouth (M), pharynx (P) and
lingual ribbon or radula (R). Approx. 30X.
Cross section of the neck region showing the larval trematode parasites (PA) inside the
large intestine; some of the gills (G) from the right side, and in the lower portion,
the cross section of the esophagus (E) and columellar muscle (C). Approx. 80X.
66 B. C. DAZO
PLATE VII. Histological section of Goniobasis livescens.
FIG. 1. Cross section of the buccal mass showing the pharynx (P), the pair of salivary glands
(S), the buccal cartilage (BC) and the complicated buccal musculature (BM). 60X.
FIG. 2. Cross section of the ovary of a female collected in the winter showing the presence of
ripe ova in the gonad.
FIG. 3. Close-up of the ovary showing a ripe ovum. Approx. 400X.
FIG. 4. Cross section of the stomach (S) showing the entrance of the single duct (D) from the
digestive gland (L). Approx. 60X.
FIG. 5. Longitudinal section of the tentacle (TE) showing the eye. Approx. 200X.
list of these algae is given in Table
15. Bacteria and soil material were
also present in the gut of G. livescens.
The large quantity of decaying vegeta-
tive material and extremely fine sand
grains in the stomach of P. acuta clearly
indicates that this animal is a substrate
feeder.
Parasites and Predators
The pleurocerid group and especially
the genera Pleurocera and Goniobasis
have long been known to serve as inter-
mediate hosts for a variety of trema-
PLEUROCERA AND GONIOBASIS 67
TABLE 15. A systematic list of algae serving as food to Pleurocera acuta and Goniobasis
livescens .
A. From stomach contents of 200 specimens each of both species, from various localities in
Michigan.
Division: CHLOROPHYTA
Sub-division: Chlorophyceae
Order: Tetrasporales
Family: Palmellaceae
Species: Sphaerocystis schroeteri Chad.
Order: Ulotrichales
Family: Microsporaceae
Species: Microspora floccosa (Vauch.) Thur.
Family: Cylindrocapsaceae
Species: Cylindrocapsa geminella Wolle.
Family: Protococcaceae
Species: Protococcus viridis Ag.
Order: Chlorococcales
Family: Oocystaceae
Species: Chlorella variegatus Beij.
Dictyosphaerium pulchellum Wood
Order: Zygnematales (Conjugales)
Family: Desmidiaceae
Species: Desmidium grevillii (Kiitz. )
Micrasterias radiata Hassall
Staurastrum furcigerum Breb.
Division: CHRYSOPHYTA
Sub-division: Bacillariophyceae
Order: Pennales
Family: Fragilariaceae
Species: Diatomella balfouriana Grev.
Tabellaria fenestra (Lyngb. ) Kiitz.
Family: Gomphonemataceae
Species: Gomphonema Vibrio Ehr.
Family: Cymbellaceae
Species: Cymbella cistula (Hempr. and Ehr.) Kirchn.
C. lanceolata (Ehr.) Brun.
Epithemia turgida (Ehr. ) Kiitz.
Rhopalodia gibba (Ehr.) O. Müller
Family: Naviculaceae
Species: Navicula gracilis Ehr.
N. radiosa Kiitz.
N. rhyngcocephalaKütz.
Pinnularia viridis (Nitzsch. ) Ehr.
Anomoeoneis sphaerophora (Kütz.) Pfitz.
Stauroneis anceps Ehr.
Brebissonia boeckii (Ehr. ) Grun.
Gyrosigma kilizingii (Grun.) C1.
68 B. C. DAZO
Division: RHODOPHYTA
Sub-division: Florideaea
Family: Chantransiaceae
Species: Batrachospermum vagum (Roth)
B. From stomach contents of 50 Goniobasis livescens from Douglas Lake, Cheboygan County,
Michigan. 23
Division: CHRYSOPHYTA
Sub-division: Bacillariophyceae
Order: Centrales
Family: Coscinodiscaceae
Species: Melosira ambigua (Grun.) O. Müll.
M. varians C. A. Ag.
Cyclotella bodanica Eulenst.
Cyclotella sp.
Cyclotella sp.
Coscinodiscus lacustris Grun.
Order: Pennales
Family: Fragilariaceae
Species: Tabellaria fenestra (Lyngb. ) Kütz.
Fragilaria brevistriata Grun.
F. capucina Desmazieres
F. construens (Ehr.) Grun.
F. construens (Ehr.) Grun. var. subsalina Hust.
Synedra ulna (Nitzsch) Ehr.
S. vaucheriae Kütz.
Family: Achnanthaceae
Species: Achnanthes exigua Grun. var. heterovalvata Krasske
A. lanceolata Breb.
A. minutissima Kütz.
A. minutissima Kütz. var. cryptocephala Grun.
Cocconeis pediculus Ehr.
C. placentula (Ehr.)
Family: Gomphonemataceae
Species: Gomphonema constrictum Ehr.
G. subtile Ehr.
Family: Cymbellaceae
Species: Cymbella affinis Kütz.
C. cymbiformis (Agardh? Kütz.) van Heurck
C. delicatula Kütz.
C. naviculiformis Auerswald
C. prostrata (Berkeley) Cleve
C. ventricosa Kütz.
Amphora normani Rabh.
Family: Epithemiaceae
Species: Epithemia zebra (Ehr.) Kütz.
Rhopolodia gibba (Ehr.) O. Müller
23Identified by Dr. George M. Davis, Mollusk Division, Museum of Zoology, University of
Michigan, Ann Arbor, Michigan.
PLEUROCERA AND GONIOBASIS 69
Species: В. parallela (Grun.) O. Müller
Family: Nitzschiaceae
Species: Nilzschia acicularis W. Smith
N. hantzschiana Rabh.
N. sinuata (W. Smith) Grun. var. tabellaria Grun.
Family: Naviculaceae
Species: Mastogloia smithii Thwaites
М. smithii Thwaites var. cryptocephala Grun.
Amphipleura pellucida. Kiitz.
Gyrosigma kützingii (Grun. ) Cleve
Stauroneis anceps Ehr.
Navicula cryptocephala Kiitz.
N. cryptocephala Kütz. var. venela (Kütz.) Grun.
N. exigua (Greg.) O. Müller
. lacustris Greg.
minima Grun.
oblonga Kiitz.
pupulla Kiitz.
radiosa Kiitz.
rostella Kiitz.
EEE FIT
. viridula Kütz.
. radiosa Kütz. var.
rhynchocephala Kütz.
tenella (Breb.) Grun.
. tuscula (Ehr.) Grun.
. tuscula (Ehr.) Grun. fo.
minor Hust.
Pinnularia lata (Breb.) W. Smith
todes. The numerous records of pleuro-
cerids as hosts of larval flukes clearly
indicate the significance of pleurocerid
biology in the field of parasitology.
For a number of larval forms the life
histories are not known, to quote only
Cercaria aurita (Zetek, 1918), a mono-
stome cercaria of the urbanensis type;
C.gorgonocephala (Heard, personal com-
munication), an interesting cercaria
forming colonies by joining tails, both
from Goniobasis livescens; as well as
a dozen species of virgulate xiphidio-
cercariae from P. acuta and G. lives-
cens and from Goniobasis sp. (Hall,
1960).
The life cycles of certain fish tre-
matodes developing in Pleurocera and
Goniobasis are, however, knownand data
from several important publications re-
lating to three families have been as-
sembled, and are included, in Table
16.
These trematodes of fishes are
remarkable in that a number of them
have a contracted, modified life cycle
in which some step in the development
of the digenetic trematodes is sup-
pressed, some species being even
capable of direct development in the
snail without passing through a verte-
brate host.
Dobrovolny (1939b) showed that G.
livescens served as both first and second
intermediate host of the allocreadtrema-
tode Plagioporus sinitsini, a parasite
of cyprinid and other fish. The cer-
cariae never leave the sporocyst in which
they form but encyst т situ. The
sporocysts with mature metacercariae
emerge from the snail to be consumed
by their definitive host.
The aspidogastrid species Cotylo-
gastev occidentalis was found to occur
in Goniobasis in 2 forms, “immature”
and “mature”, the latter containing
numerous eggs with viable embryos
(miracidia) (Dickerman, 1948). That
author further stated that, while it was
possible to infect sheephead (Aplodinotus
70
TABLE 16.
B. C. DAZO
Definitive Host
Trematode infections observed in Pleurocera acuta and Goniobasis livescens
Parasite Intermediate Snail Host (Vertebrate and Author
Invertebrate)
Cercaria aurita Goniobasis pulchella (-lives- |No data Zetek, 1918
cens)- Big Vermilion River,
Illinois.
Plagioporus G. livescens, Oneida Lake, Fishes Baker, E.C., 1916
sinitsini New York
Plagioporus G. livescens, Huron River, Cyprinid and other |Dobrovolny, 1939b
Sinissini huroni |Washtenaw Co., Michigan fishes
Plagioporus G. livescens, Huron River, Centrarchid fishes |Dobrovolny, 1939a
lepomis Washt. Co., Mich. 1.25% of
No specific
trematode given
43,189 snails shed cercaria
Pleurocera acuta Outlet of L.
Oconomowoc, Wisconsin.
(Oconomowoc River)
No data
Baker, F.C., 1928a
Proterometra G. livescens correcta-Des Fishes: Dickerman, 1934
macrostoma Plaines River, Evanston and Crappie, Pomoxis
Hickory Creek, New Lenox, Sparoides; blue
Illinois gills, Helioperca
incisor; sunfish,
Eupomotis gibbosus
Proterometra Р. acuta and С. livescens from Fishes Dickerman, 1934
macrostoma the Great Lakes Region.
Proterometra P. acuta and G. livescens W. Dickerman, 1945
Sagittaria Lake Erie, Sandusky River, Sunfish,
Freemont and Maumee River, | Eupomotis gibbosus
Ohio
Cotylogaster С. livescens-Bass Is. , Lake Fishes: Dickerman, 1948
occidentalis Erie, Ohio. 2% of 7,697 snails} Rock bass, Amblo-
infected. plites rupestris;
sheephead, Aplo-
dinotus grunniens ;
clam, Lampsilis
luteola
Cercaria G. livescens , Douglas Lake, No data Heard (1960)
gorgonocephala {Cheboygan Co., Mich. (pers. comm.)
virgulale С. livescens and P. acuta fr. | No data Hall, 1960
xiphidiocercariae
(12 species)
Wabash and Tippecanoe rivers,
Indiana, and Goniobasis sp. fr.
Marquette river, Michigan
possibility of developing within or with-
out a vertebrate host, he supported the
classification which places the Aspido-
gastrea in a trematode subclass distinct
grunniens) experimentally by forcible
feeding of these eggs, the embryosinthe
egg were not dependent upon the fish for
continued existence. Because of this
PLEUROCERA AND GONIOBASIS 71
from the Digenea. This fluke has also
been reported from a clam.
Similar conditions seem to prevail
among the Azygiidae, whose large cysto-
cercous cercariae are known to be eaten.
by centrarchid fishes, in which they
mature. According to Dickerman (1946)
the rediae of Proterometra sagittaria,
after discharge of cercariae, also con-
tained eggs with mature miracidia, which
likewise suggests the possibility of an
alternative direct life-cycle. Parallel
observations were made for Protero-
metra macrostoma by Anderson (1962,
personal communication).
Parthenitae and cercariae of certain
trematodes were frequently encountered
in the course of this study in snails
from various localities in Michigan. The
cercariae of Proterometra macrostoma
were found in G. livescens collected in
the Ocqueoc River, Presque Isle County,
northern Michigan, as well as Portage
Creek and Zuckey Lake Inlet, south-
eastern Michigan. In the same region
this parasite was also found in P. acuta
from Portage Creek and Honey Creek.
Some P. acuta collected from the Big
Pigeon River, Ottawa County, south-
western Michigan, shed Cercaria sagit-
taria; Plagioporus sinitsini cercariae
were shed by G. livescens collected in
the Huron River and Kalamazoo River
stations.
These various parasites were foundin
the liver, gonad, alimentary canal
(especially the large intestine or rectum)
and the mantle region in the vicinity of
the laminal folds of the “open” or
terminal portion of the reproductive
tract of the snail.
Information about animals that prey on
pleurocerids is rather scarce, but it
appears that many pleurocerids are
consumed by fishes. For example,
Dickerman (1948) examined 22 sheep-
heads and found evidence in the stomach
of one large fish that it had eaten
Goniobasis snails. The fish was also
parasitized with 3 specimens of Cotylo-
gaster occidentalis, which it may have
thus acquired. Goodrich (1945) reported
that an examination of the stomach con-
tents of brook trout (Salvelinus fontin-
alis) yielded the remains of shells of 8
genera of fresh-water mollusks, in-
cluding G. livescens and that shells of
that species were found in the gizzard of
a white-winged scoter shot at Fish Point,
Tuscuola County, in 1926.
DISCUSSION OF PLEUROCERID
SYSTEMATICS
While there are some striking differ-
ences in the morphology of the she1124
and operculum of P. acuta and G. lives-
‘cens (Summarized in Table 17)andsome
distinction in the radular teeth, there
is a striking similarity in the internal
anatomy of the 2 species. Despite some
differences in ecological preferences
and in other detail, the general pattern
in the life history of both species is
almost identical. A consideration of
these basic similarities emphasizes that
P. acuta. is closely related to G. lives-
cens, and indicates that the present
systematic arrangement, with each
Species under a separate genus is open
to question. Evidently the use of shell
characters alone in this group, where
intra- and inter-specific variation is
so common, does not seem to provide
a good criterion for intrafamilial
classification.
While the present systematic arrange-
ment appears unsatisfactory, it is not
yet possible to submit a better one. The
Pleuroceridae have been and will
probably continue to be a difficult group
to contend with, because few thorough
and inclusive morphological and bio-
logical studies have yet been made,
while such knowledge as we have does
indicate great morphological simi-
larities of the animals. The system-
atic uncertainties exist at all levels and
are due in part to unfortunate legacies
24 There were, however, some intermediate
specimens from the field in which these
differences were hardly discernible.
72
Feature
Adult shell
Juvenile shell
Operculum
Radular teeth
B. C. DAZO
Elongated; whorls flat numbering
from 9to 11; no callus thickening on
parietal wall; columella twisted;
aperture angulate tending to form a
canal below.
Double carinae prominent on the
whorls. In adult shells these ridges
are present only in the first 3to 6
whorls; lateral ridge less marked
thanthe median; sometimes 3 carinae
may be found in some specimens, 1
median and 2 lateral.
Small; more elongated and thin; more
uniform in shape; spaces between
growth scars
growth lines narrow;
well marked by dark lines.
Range of cusps
in lst marginal
in 2nd marginal
TABLE 17. Comparison2° between Pleurocera acuta and Goniobasis livescens
Pleurocera acuta
Goniobasis livescens
Ovately conic; whorls more convex
ranging from 7 to 9; parietal wall
with callus; columella smooth; aper-
ture subrhomboidal, subangular at the
base but not canaliculate.
Single carina present at the middle of
juvenile whorls; this ridge usually
disappears in matured specimens but
is sometimes retained.
Larger and more variable in shape;
wide spaces between growth lines
which under the microscope appear
as very fine spiral lines and are
similar to wrinkled ridges as in the
sculpture of many fresh-water shells.
6-7
8-12
Teeth, though equal in size,
relatively much larger.
Lives in almost any kind of clean,
permanent type of fresh-water envi-
ronment ranging from springs to
Ecology Generally inhabits quiet areas in big-
ger streams; prefer sandy-muddy
bottom presumably because of its
burrowing habit.
Egg-laying In masses.
swift flowing streams and rivers and
sheltered areas in lakes; prefers to
crawl on rocks or stones. |
Singly.
25The difference in size is not considered an essential feature.
left by pioneer workers such as Rafin-
esque, Lea and many others (Walker,
1917) (see introduction, p 9).
Only recently has there been an em-
phasis on the value of morphological,
as well as life history studies, in evalu-
ating the phylogenetic relationships
among animals in most molluscan
groups, including the pleurocerids.
Morrison’s (1954) attempt to regroup
the North American pleurocerids
according to the characteristics of their
egg masses opens interesting possi-
bilities. He has assigned the name
Oxytrema to those forms whose egg
capsules aggregate in clusters and are
usually encased in sand grains, and he
includes all species hitherto known as
Pleurocera and most species known as
Goniobasis. The pleurocerid species
whose eggs are laid singly or instraight
chains (including Goniobasis livescens)
he relegated to the genus Mudalia. How-
ever, observations do not yet exist for
all species and it is not certain whether
egg-deposition characteristics will ulti-
mately prove to be a valid criterion at
the generic level, or perhaps only at
PLEUROCERA AND GONIOBASIS 73
the specific level.
On the basis of what was known about
reproductive features, such as egg-
masses and spermatophores, Rosewater
(1960a) divided the pleurocerids into
5 categories, which were ‘‘inpart corre-
lated with the ecologic niche in which
each species is found.” Later, Rose-
water (1961) indicated the possible
taxonomic implications of the differences
he found in the length of the commis-
sures and connectives of the central
nervous system of 9 species of Pleuro-
ceridae. Since the 3 species of pleuro-
cerids belonging to 3 genera (Pleuro-
cera, Goniobasis and Jo that I have
examined in this respect proved to be
very closely similar and since ex-
amination did not corroborate the differ-
ences indicated, this attempt at classi-
fication does not appear valid.
The information obtained in this study
would seem to favor a classification
based on the character of the egg masses.
As shown in Table 9, information is
available at the present time for 12
Species. From these data it is now
possible to formulate some tentative
group relationships. The groupings here
proposed are:
(1) Eggs in batches or compound
masses; conspicuously cased in
sand grains. This group includes
Pleurocera and some species of
Goniobasis.
(2) Eggs laid singly, sometimes con-
nected by strands of outer egg-
membrane (up to 6 in a row),
with shell membrane covering and
a thin layer of soil. Anculosa,
and the majority of the species
of Goniobasis belong in this
category.
(3) Eggs laid in pairs opposite each
other in a continuous ribbon-like
mass. Lithasia is the only known
member of this group.
(4) The eggs are arranged in rows,
up to 5 in arow, running diagonally
across the elongated gelatinous egg
mass. This group includes Jo
fluvialis and presumably its forms.
It is expected that additional infor-
mation about the character of egg
deposition of the other genera will enable
a more complete and accurate analysis
of the value of this feature for deter-
mining group relationships. However,
such reproductive characters are not
sufficient in themselves and must be
Supported or supplemented by a variety
of other significant biological data. For
example, the host specificity indicated
by a Similarity in larval trematode in-
fection may also prove useful in any
attempted reclassification of these
snails.
Cytological and electrophoretic
studies might also throw light on various
relationships. But, in the present state
of knowledge it is impossible to appreci-
ate which combination of features would
be most useful in an evaluation of the
systematics of the group. It hasbecome
increasingly obvious, however, that many
more basic studies are needed on the
morphology and biology of members of
the Pleuroceridae to derive more mean-
ingful and concise taxonomic arrange-
ment of the genera and species now
grouped within this family.
ACKNOWLEDGMENTS
I wish to express my sincere gratitude
to Dr. Henry van der Schalie, whose
continued guidance, encouragement and
unfailing interest in my work made this
study possible. Grateful acknowledge-
ment is also made to Dr. J. B. Burch
for constant advice and aid during the
course of the investigation and for
accompanying me on several field trips.
I am also indebted to Dr. Nelson G.
Hairston, whose kind assistance and
constructive criticisms aided me during
the formative stages of this work; to
Mrs. Anne Gismann who critically edited
the manuscript, and to Mr. William L.
Brudon and Mrs. Stanlee Lonsdale for
their help in the preparation of figures
and plates.
74 B. C. DAZO
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RESUMEN
HISTORIA NATURAL Y MORFOLOGIA DE PLEUROCERA ACUTA
RAFINESQUE Y GONIOBASIS LIVESCENS (MENKE)
Relativamente poco es lo que se conoce acerca de los Pleuroceridae, una familia
de caracoles fluviales operculados comün en Norte America, la cual comprende,
o esta relacionada con, caracoles melanidos de importancia médica en el Lejano
Oriente. La taxonomia, principalmente basada en caracteristicas concholögicas,
necesita una revision general. Aqui se estudiala morfologia y biologia comparadas
de dos especies clasificadas en géneros diferentes: Pleurocera acuta Rafinesque
y Goniobasis livescens (Menke) procendentes de cuatro estaciones cerca de Ann
Arbor, Michigan, y de otras localidades adicionales en Michigan y en Ohio.
Aunque opérculos y concha en estas dos especies son diferentes, las similari-
dades encontradas en sus anatomias internas asi como en los modos de vida son
tan extraordinarias que su ubicación en géneros diferentes resulta cuestionable.
Diferencias conchológicas, a veces muy marcadas, no estan siempre presentes
y en algunos especímenes son poco discernibles. P. acuta es doble entamaño; aun-
que la forma general y pigmentación del cuerpo son similares, P. acuta tiene la
trompa y región anterior del cuerpo más alargados, con tentáculos largos. El pié
es más alargado pero en proporción más pequeño lo cual puede ser una adaptación
a la vida de fondo y hábitos excavadores, mientras que G. livescens tiene el pié
80
B. C. DAZO
mäs redondeado y grande en relaciön a la cabeza, lo que puede asociarse con sus
hábitos reptantes. Manto y órganos sensoriales, organización general del sistema
nervioso, morfología de los aparatos respiratorio, digestivo, excretor, circulatorio,
y el sistema muscular de ambas especies son muy similares, y difieren sólo en
tamaño. En los Pleurocerinae, el macho no tiene órgano copulador; las hembras
tienen una cavidad reproductiva en el cuello entre el tentáculo derecho y la base
del pié, y una hendidura poco profunda que conduce a esa cavidad. En otros aspec-
tos el sistema reproductor corresponde en general conel de los demás prosobran-
quios. Los sexos son separados. En ambas especies los órganos reproductores
de cada sexo son casi idénticos, ocupando la misma posición. Los espermatozoos
son de dos tipos: eupirenos, típicos, y los apirenos, atípicos; los últimos se trans-
fieren a la hembra mediante espermatoforos.
. Ecologicamente los pleuroceridos norteamericanos requieren aguas claras. Ex-
ceptuando Goniobasis todos prefieren habitats amplios. Usualmente viven en fondos
de arena o barro en áreas al abrigo de las corrientes Goniobasis livescens se
encuentra en casi todos los ambientes dulceacuícolas limpios de tipo permanente
(manantiales, lagos, rápidos) y con frecuencia se encuentran crepando en rocas.
Observaciones en el ambiente natural y en el laboratorio indican que el aparea-
miento tiene lugar en otoño. Cuando la temperatura desciende a menos de 5%C
los animales invernan, y la actividad es reasumida, comenzando a desovar, en la
primavera. Los huevos de P. acuta se depositan en masas cubiertas de arena, de
diferente forma y tamaño, y el número de huevos por masa varía entre 1 y 19.
G. livescens pone los huevos de uno a uno, algunas veces dos o tres seguidos, pero
depositados varios centimetros aparte y generalmente quedan cubiertos con una fina
capa del substrato. P.acuta produce más huevos diarios (15) que С. livescens
(4), pero tiene un período de puesta más corto, de abril a junio (G. livescens de abril
hasta mediados de agosto). El crecimiento es más pronunciado durante el primer
año (de 0.3 a 10 mm en P. acuta; 0,3 a 3,8 mm en С. livescens). Cuando los са-
racoles criados en el laboratorio alcanzaron madurez sexual a los dos años, el
tamaño era de 16,7 y 7 mm de largo respectivamente, despues de lo cual no se
observó crecimiento apreciable. Caracoles de ambientes naturales eran más grandes.
La duración normal de la vida es tres años, pero quizá pueda extenderse a cuatro.
En P.acuta la proporción de sexos es de dos a uno en favor de las hembras, y en
G. livescens es de cinco a uno.
Como otros prosobranquios, ambas especies de alimentan de algas verdes y
rojas, desmidos y diatomeas.
Larvas de trematodes, principalmente de Azygiidae, Allocreadiidae y Aspido-
gastridae, con frecuencia y abundancia parasitan el hígado, gonada, canal alimenticio
y otros órganos.
MALACOLOGIA, 3(1): 81-102, 1965.
GROWTH AND STUNTING IN ONCOMELANIA
(GASTROPODA: HYDROBIIDAE)!
Henry van der Schalie and George M. Davis
Museum and Department of Zoology
University of Michigan, Ann Arbor, Michigan, U. S. A.
ABSTRACT
These data deal with the problem of raising large numbers of Oncomelania
spp. rapidly, efficiently and in a predictable way as a means for facilitating
studies of Schistosoma japonicum in the laboratory. Previous reports indicate
that the growth rates attained in other laboratories were about 0. 3-0.4 mm per
week under conditions that produced excessive mortality (38% in one publication).
The culture procedures here described stimulate fairly uniform growth rates
of about 0.65 mm per week with a mortality rate below 10%. Optimal growth is
obtained when 1 or 2 young newly hatched snails (2. 0-2.5 whorls) are placed in
a 9 cm Petri dish. A patty of unsterilized mud, which is alkaline, fine textured
and supports the growth of naturally occurring diatoms, is placed in the center
of this dish. After the addition of water, the dish is covered and placed under
light of about 150 foot candles cycled for about 10 to 12 hours per day. No food
additives are used; the temperature is maintained at about 250 3 20C.
Increasing the number of snails per culture to 5 and 10 caused stunting,i.e.,
a distinct decrease in the rate of growth and development. Correlated with
stunting was a decrease in the rate of gonadal maturation, a lack of development
of the sex organs, and an increased mortality. The shell of the stunted snail is
indistinguishable from that of a normal one; consequently, the dwarfed snail can
only be identified if one knows its age.
' Optimal growth is dependent on the interaction of the following variables:
light, an adequate volume of container, suitable soil and a thriving microflora.
When the light and the volume of the container are kept constant, a soil high in
calcium and capable of supporting an abundance of green algae and diatoms is
most critical.
INTRODUCTION
Two major difficulties encountered
in studying Schistosoma japonicum in
laboratories far removed from endemic
areas are: 1) the length of time neces-
sary for the parasite to mature in the
snail; 2) dependable and efficient methods
for rearing species of Oncomelania,
so that a sufficient supply of snails
of uniform age and size for full scale
experiments will be assured. Because
of these difficulties studies on 5.
japonicum have lagged far behind simi-
lar investigations involving S. mansoni.
The latter matures in Australorbis gla-
bratus in about 1 month. Ritchie et al.
(1963) have shown that A. glabratus can
also be grown from the egg to maturity
in one month. In comparison 5.
japonicum matures in Oncomelania in
3-4 months and the time reported for
growth from egg hatching to maturity
for species of Oncomelania is gener-
ally in excess of 5 months (DeWitt,
1952).
In our program, culture techniques
have been developed which enable not
1This work was carried out under the sponsorship of the Commission on Parasitic Diseases,
Armed Forces Epidemiological Board; and was supported by the Office of TheSurgeon General,
Department of the Army.
(81)
82 VAN DER SCHALIE AND DAVIS
only a predictable high rate of production
but also a means for insuring a rapid
rate of growth and maturation with a
minimal rate of mortality for the 4
so-called species of Oncomelania. In
an attempt to increase efficiency in
rearing young snails we increased the
density of the young snails per culture.
It was found that this crowding caused
a pronounced degree of stunting, which
was evident not only in terms of a de-
creased rate of growth but also in a
decreased rate of maturation of the
reproductive system. The latter was
demonstrated in histological and ana-
tomical studies.
Dwarfing among various organisms
raised under crowded and unsuitable
environments has been observedfor well
over 100 years. While such stunting
has been studied in several aquatic
pulmonate snails, the fact that it also
occurs in amphibious prosobranchs has
not been previously demonstrated. A
more comprehensive review of the lit-
erature dealing with stunting of aquatic
snails can be obtained inthe publications
of the following authors: Colton, 1908;
Forbes and Crampton, 1942; Chernin
and Michelson, 1957 a,b; Wright, 1960;
Berrie and Visser, 1963.
The purpose of this paper is to
demonstrate: (l) the culture conditions
which produce optimal growth in young
Oncomelania; (2) the effects of crowding
on growth and development of O. for-
mosana; and (3) the necessity for
understanding the relationship between
the size and age in species of On-
comelania. This informationisprovided
to demonstrate that adequate criteria
for measuring optimal physiological
conditions and normal growth are neces-
sary in experiments which involve inter-
mediate hosts in the many phases of
schistosomiasis research. For example,
it should be understood that among
stunted snails neither size nor maturity
is related to the actual age of those
snails. Furthermore, one cannot tell
a normal snail from a stunted snail
on the basis of its shell alone. These
data are designed to provide an ade-
quate means for detecting the kinds of
environment and the conditions which
usually cause stunting.
MATERIALS AND METHODS
Snails studied
Stunting was observedinO, nosophora,
O. formosana, and O. hupensis;however,
O. formosana only was used for the
more intensive studies and experiments.
All of the snails were laboratory reared
young which were removed from paren-
tal cultures at about 1 week of age,
when they had 2.0-2.5 whorls. At
2 whorls the height of the shell was
about 0.5 mm. The young were then
placed in the different types of culture
chambers where they were maintained
for at least 8 weeks.
Culture chambers
It has been generally recognized that
the young of Oncomelania tend to be
aquatic and are usually found submerged
in the water provided in their aqua-
terraria for at least 2 weeks of their
early development. Taking this tendency
into consideration, 2 types of cultures
were used for rearing the young; a
plastic tray culture and a Petri dish
culture. The former was modified from
the aquaterrarium used by DeWitt
(1951, 1952) and closely resembles that
developed by Moose and Williams
(Moose, personal communication, 1964).
This container is a moulded plastic tray
often used by florists as planters.
The tray is 11” x 7.5” x 2.5” BBicmı
19 cm x 6 cm). The soil used was ob-
tained from the habitat of Pomatiopsis
cincinnatiensis, a North Americar
amphibious snail related to Oncomelania.
This soil was alkaline and supported
a high level ofalgalproductivity (green
algae and diatoms). Its texture varies
as follows: sand, 40-69%, silt, 13-42%;
clay 7-24% (van der Schalie and Getz,
1962). It was found that the cultures
were maintained much better if the soil
GROWTH AND STUNTING IN ONCOMELANIA 83
had a minimum of sand. The soil
was smoothed into a firm, flat, rectan-
gular mass at one end of the tray
giving an area of about 45 square inches.
The edge of the mass sloped at a
25° angle into the reservoir. The
depth of soil was 0.5 - 0.75 inches.
This reservoir was filled with about
200 cc of boiled, filtered pond water
and the tray was then covered with a
sheet of plexiglass. The central area
of the cover was bored with 160-170
holes, each 2.5 mm in diameter, which
provided for gaseous exchange and the
escape of some water vapor. A 1
cm hole was drilled through the lid to
provide access to an area over the
reservoir. This opening served to
accommodate an aeration tube. The
reservoir was actively aerated at all
times.
The culture thus prepared was then
heated in an oven at 600 C for 2 hours;
this baking eliminated a problem often
caused by oligochaetes, without killing
the algae. In unheated cultures the worms
tended to “tear up” the soil with
their burrowing activity so that, within
a week, their presence was evident by
isolated piles of worm castings. Usually
within a month at least 80% of an
untreated culture was seriously disrup-
ted because of worm activity.
The Petri dish culture chamber
has an inside diameter of 9 cm and
a depth of 1.9 cm. A mound of mud,
from the source previously mentioned,
was placed in the center of the dish
where it was stroked with a spatula
to form a smooth and solid surface.
This mound was 1.5 cm high and it
had a basal diameter of 6 cm. A
clear and open space of 1.5 cm was
left between the glass wall and the
base of the soil mound and it served
as a reservoir to which about 40 cc
of pond water was added. These cul-
tures were not baked since such a
small amount of soil does not harbor
a sufficient number of worms to cause
any appreciable damage to the culture,
and since such cultures were used for
only 8 weeks. The dish was finally
covered with the usual petri dish cover.
Active aeration is not necessary.
Both types of cultures were illuminated
for 10-12 hours daily by a 40 watt,
white, ‘‘cool,’’ fluorescent tube with an
intensity of 100 to 150 foot candles,
suspended 10 inches above the cultures.
The radiation from the light maintained
the temperature in the Petri dish cul-
tures at 25°C + 20; that of the plastic
tray cultures at 249 t 20C.
EXPERIMENTS
The Effect of Light on Growth
For all 4 of the so-called species
of Oncomelania it was found that growth
was fastest when a single young specimen
was placed in a Petri dish and the
culture was maintained under light. This
development is shown in the following
experiments with O. formosana.
Two experiments (la and 1b) were
designed to determine the effect of light
on the survival and growth of young
O. formosana, which differed only in
that one was terminated in 7 weeks,
the other in 8. In each case 3 groups
of 50 snails each (2.0-2.5 whorls) were
arranged, as follows: one group was
placed in constant dark (pitch-black),
a second in constant light, and the third
in normal, natural, room-level light;
these snails were maintained singly in
Petri dishes.
The intensity of the constant light
varied from 100to 125 foot candles;
the variance depended on the distance of
the dish from the light source. Room-
level intensity varied from 35 to 45
foot candles during the day and was
reduced to about 10 at night. The
temperature: for cultures maintained
in the dark and room-level light was
24° + 2° С Че. оу 1°C less than
those exposed to the radiation warmth
of the light. At the end of each ex-
periment the snails were removed, their
sex determined, weight and length mea-
sured, and the percentage of survival
84 VAN DER SCHALIE AND DAVIS
calculated. The results are shown in
Table 1.
The data showed that the most rapid
growth occurred in snails maintained
under constant light. During the ex-
periment lasting 7 weeks, males grew
0.77 mm per week and females 0.80.
By the 8th week the logarithmic phase
of growth was over and little further
increase could be expected. In the ex-
periment covering 8 weeks, males main-
tained under constant light had grown
with a rate of 0.68 mm per week and
the females 0.78. Males and females
maintained in the dark or at room-
level light for the 7 weeks had growth
rates of about 0.44 and 0.39 mm per
week, respectively.
In the experiment lasting 8 weeks,
rates of growth were increased only
for snails maintained in the dark or
room-level light. Males and females
in the dark grew with a rate of about
0.49 mm per week while males and
females in room-level light grew with
rates of about 0.60 mm per week.
The increase in growth rate for snails
maintained 8 weeks under room-level
light over that of snails maintained 7
weeks in the same environment was
most likely due to variability in the
fluctuation of light in the room-level
light situation as well as a slight growth
spurt in the 8th week in the second
experiment.
The relatively high mortality rate of
snails reared under constant light was
due, in part, to the detrimental effects
of algal accumulation in the cultures.
Constant light induced algal proliferation
with the following negative effects: (1)
algae overgrew young snails, hindering
movement and causing death; (2) dense
algal mats tended to limit the soil sur-
faces for browsing; and (3) living snails,
which were often covered with algae,
were difficult to find. Although growth
rates were maximal under full 24-hour
illumination, it was concluded that this
advantage was offset by disadvantages
of too luxuriant a proliferation of fila-
mentous algae and that better balance
TABLE 1. Differential growth and survival of Oncomelania formosana reared singly in Petri
dish cultures under different conditions of lighting
Experiment la
Sex ration 2/3
Average wt in gm*
Average length in mm
Percentage survival
Experiment 1b
Sex ratio
Average wt in gm*
Average length in mm
Percentage survival
*including shell
o - Standard deviation
: Snails reared 7 weeks
Snails reared 8 weeks :
Dark Constant
1/0.78 1/0. 81 141.3
0. 0062 0. 0054 0. 0208
0. 0068 0. 0059 0. 0227
3. 5(01. 07) 3. 0(01. 20) 5. 9(00. 15)
3. 6(01. 02) 3. 3(00. 29) 6. 1(00. 21)
57 88 76
1/0.55 1/1. 05 1/13
0. 0089 0. 0127 0. 0191
0. 0114 0. 0162 0. 0273
4. 3(01. 35) 5. 2(00. 28) 5. 9(a0. 14)
4. 6(01. 48) 5. 3(60. 39) 6. 7(00. 15)
48 82 64
GROWTH AND STUNTING IN ONCOMELANIA 85
TABLE 2. Mortality in 2 series of Oncome-
lania formosana cultured in Petri
dishes at varying densities
No. snails | tality at
used
Experiment
between development and survival might
be obtained by shortening the duration
of direct illumination. As will be seen
in subsequent experiments where the
duration of light was reduced to 10-
12 hours per day, there was a decreased
algal growth with a decided decrease
in mortality.
The data appear to show that increased
temperature is correlated with an in-
crease in the growth rate. It is not
yet possible in this paper to discuss
quantitatively how light, temperature,
and food supply interact to provide an
environment for optimal growth. How-
ever, it is already evident that tempera-
ture differences per se between 24°C
and 26°C were not sufficient to account
for the observed differences in growth.
The Effect of Population Density on
Growth.
We were anxious toincrease efficiency
by rearing more snails per area; to
this end, 2 series of experiments (A
and B) were set up. The snails were
kept in Petri dishes under equal and
optimal environmental conditions (10-
12 hours of light daily), only the number
of snails per dish varied. At the end
of 8 weeks (1 group at 9 weeks) the
snails were removed from culture and the
length of shell, sex, and whorl count
were recorded for each snail. A sub-
sample was chosen at random; the speci-
mens were fixed in Bouins, sectioned,
and stained with Hematoxylin and Eosin.
These sections were then analyzed for
degree of gonad development.
TABLE 3. Comparative growth of Oncomelania formosana cultured in Petri dishes at varying
densities, at 8 weeks
pene se
$
$
8
№. snails
рег dish
2А
5.8 7.0 0. 65
3.7 5.9 0.40
2.7 5.1 0. 25
5.8
3.8
3.1 -
5.8 6.9 0. 66
4.0 5.7 0. 44
2.7 4.9 0. 28
1
5
10
il
5
10
2B d 2
$ 5
$ 10
2
5
10
Average
No. of Growth in
Whorls mm/week
6.8 0.56
5 5.9 0. 41
3 5.3 0. 39
86 VAN DER SCHALIE AND DAVIS
NUMBER OF SNAILS
Ne BE A re,
10 Per Dish
..
.....
.
5 Per Dish
1 Per Dish
0 1 2 A S 6 PIS
LENGTH OF SHELL IN MM
FIG. 1. Histogram showing growth in terms of size distribution among Oncomelania formosana
cultured at 1, 5 and 10 per Petri dish for 8 weeks. (Experiment 2A).
Experiment 2A. Young snails (2.0-
2.5 whorls) were reared in Petri dishes
with 199 reared singly, 340 distributed
in groups of 5 per dish, and 450 main-
tained at 10 per dish. When the snails
were removed from culture after 8
weeks and the data tabulated, the effects
of increased density were pronounced.
Crowding resulted in increased mor-
tality (Table 2). It also produced a
distinct decrease in shell size and whorl
count. The average length of shell,
the whorl counts for the males and
females, as well as their average rates
of growth for the 8-week period are
tabulated in Table 3. The distributions
around these mean values are given
in Figs. 1 and 2.
The average growth rate for snails
reared singly was 0.56 mm per week
for the males and 0.65 mm per week
for the females. Under conditions of
crowding this rate was only 0.41 and
0.40 for males and females, respectively,
when the animals were reared at 5
snails per dish; and did not exceed
0.39 and 0.25 for males and females,
respectively, at a density of 10 per
dish.
A histological study of the gonads
GROWTH AND STUNTING IN ONCOMELANIA 87
10 Per Dish
>
о
w&
о
20
NUMBER OF SNAILS
5 Per Dish
1 Per Dish
ie Gy ORC a
ER
Thi N E
7:8
NUMBER OF WHORLS
FIG. 2. Stunting as shown by a decrease in the number of whorls of Oncomelania formosana
when males and females were maintained for 8 weeks at 1, 5 and 10 per Petri dish
(Experiment 2A); size distribution is shown in Fig. 1.
in a random series of snails from
these 3 groups indicated that the degree
of maturation was correlated directly
with the size of the snail. For purposes of
analysis each serially sectioned snail
was assigned a rating into one of the
4 following categories of gonad tissue
growth: undifferentiated, differentiated,
almost mature, and mature.
In the undifferentiated group (Fig. 3A)
gonadal tissue was either entirely lacking
or the primordia observed could not be
positively identified as gonadal tissue.
The differentiated series (Figs. 3B, C,
D) included those developmental stages
ranging from the first recognizable gonad
tissue to the initial formation of oocytes
or primary spermatocytes. The gonads
88 VAN DER SCHALIE AND DAVIS
GROWTH AND STUNTING IN ONCOMELANIA 89
which were almost mature (Figs. 3E,
G) contained secondary spermatocytes,
spermatids, and a few scattered mature
sperm in the male; in the females the
oocytes were developed to about half-
size. The fully mature gonads (Figs.
3F, H) were usually packed with mature
sperm or well developed oocytes.
In the case of the males, snails 3
mm or less in length were usually
“undifferentiated” or barely “differen-
tiated,”, while those 3.0-4.2 mm long
were “almost mature;” among those
larger than 4.2 mm, some 64% were
“mature.” It was of interest to find
that some snails were still “almost
mature” when they were 6.0 mm in
length. In any case, development was
distinctly slower in the females; snails
4.4 mm and smaller were “undifferen-
tiated” or just “differentiated;” among
those measuring 4.5 mm-5.5 mm only
50% were “differentiated;” 33% “almost
mature,” and17% “mature.” These data
were collected with respect to size only
and not by the culture condition in which
they were maintained. Correlations
of gonadal development with each culture
condition are discussed in the next ex-
periment.
Experiment 2B. While experiment 2A
was in progress we noticed that 2 young
snails per Petri dish apparently grew
as rapidly as 1 per dish. The experiment
was then repeated by placing 92 snails
at 2 per dish, 100 at 5 per dish, and
100 at 10 per dish. As in the previous
experiment, snails were removed from
culture at the end of 8 weeks for collect-
ing data excepting 16 of the snails
reared 2 per dish, which were continued
in culture for an extra week. As shown
in Table 2 analogous mortality rates
occurred in the 2 experiments. Like-
wise, the mean lengths and whorl counts
for each group of snails (Table 3)
were of the same magnitude. The varia-
tions around these means are shown
graphically in Figs. 4and5. Considering
the average growth in mm per week
for the 8-week period (Table 3), males
reared 2 per dish had a greater rate
of growth compared with those 1 per
dish, the former being 0.66 and the
FIG. 3. Differences in gonad development and maturity of Oncomelania formosana reared under
varying conditions of crowding in 8 week old males (A, B, C, E and F) and females
(D, G and H).
A. Male with an undifferentiated gonad (arrow) which could be either a male ora
female (greatest width at middle of whorl 180 u).
Differentiated gonad with male tissue just forming in a strip about 25 y wide.
C. Male tissue differentiated to form spermatocytes (greatest height of gonadal lobe
40 u).
D. Differentiated female gonad with lobes just forming (lower arrow, oocyte 35 u long).
The early stages in differentiation in the female appear similar to those for males
in B.
E. Almost mature male with spermatids and a few scattered sperm in the sections
(gonadal tissue 200 и high).
F. Fully mature male with spermatids and clusters of sperm; arrow points to a mass
of sperm 43 y in diameter.
G. Almost mature female gonad with lobes filled with oocytes in early stages of
development; some have little yolk (right arrow shows one 28 u in diameter), others
have accumulated yolk (left arrow).
H. Fully mature female gonad with gonad with eggs full of yolk (arrow indicates an
oocyte 78 y long).
90 VAN DER SCHALIE AND DAVIS
NUMBER OF SNAILS
10 Per Dish QE
5 Per Dish
2 Per Dish
0 1 Ри A 7
LENGTH OF SHELL IN MM
FIG. 4. Histogram showing growth in terms of size distribution among Oncomelania formosana
cultured at 2, 5 and 10 per Petri dish for 8 weeks (Experiment 2B).
latter 0.56, while the females at this
density level had an almost equal rate:
0.66 against 0.65. The rates ofdevelop-
ment in the snails reared at greater
densities were also quite similar in
the 2 experiments.
Results of the histological analysis are
presented in Table 4. Of the gonads
among those snails reared 2 per dish
none was “undifferentiated,” 23% were
“differentiated,” 45% were “almost
mature” and 29% were “fully mature,”
The extra week of development for the
16 snails (13 were sectioned) also pro-
duced an increase in maturation so that
39% were “almost mature” and 61%
“fully mature.” At the end of 8 weeks
more than 80% of the snails reared
5 and 10 per dish had “undifferentiated”
gonads. It is concluded that a popula-
tion of 1-2 snails per 9 cm diameter
Petri dish is vastly more favorable
in every respect than one of 5 or 10
snails per dish.
The Effect of Population Density on
Development, in Plastic Tray Cultures
The plastic trays had, for a long
period of time, proved suitable for
maintaining adults; they were also fairly
GROWTH AND STUNTING IN ONCOMELANIA 91
Experiment 2
10 Per Dish
5 Per Dish
NUMBER OF SNAILS
2 Per Dish
DIAZ AB 2487576, 7280) 12.345 7
NUMBER OF WHORLS
FIG. 5. Stunting as shown by a decrease in the number of whorls of Oncomelania formosana
when males and females were maintained for 8 weeks at 2, 5 and 10 per Petri dish
(Experiment 2B); size distribution is shown in Fig. 4. :
adequate in encouraging the production area.
of young. A tray provides about 8 x To ascertain whether the increased
the total area of a Petri dish and, surface area of soil and water would
when established, about 19 x as much provide an environment stimulating op-
soil surface area above the water line timal growth for a large number of
with about 4 x as much water surface young snails, 100 young snails were
92 VAN DER SCHALIE AND DAVIS
TABLE 4. Comparison of the effect of different conditions of culture on the gonadal develop-
ment of Oncomelania formosana
State of Gonad
Experi- | Type of Snails |Duration of
ment culture per of A Undiffer- | Differ- | Almost
eulture culture entiated | entiated | mature
Petri dish
cad
8 months
6 months
& & 3 eZ
Petri dish 2 months
8 months
TABLE 5. Showing arrested growth and mortality in a group of 100 Oncomelania formosana
raised in common, and the favorable effect of subsequent separation and culturing in
pairs
Petri dishes
for last 2 months
6+2 = 8 months
(b)
Plastic | Plastic Tray Culture = Culture
*87 snails split into 2 groups: (a) 43 to a new tray culture; (b) 44 at 2 per dish to Petri dishes.
No. snails at end of given period of
time
Average length (mm)
Average whorl count
% Mortality
87*
2.7
5. 0
6
FIG. 6. Growth differences in both size and whorlcount among a population of Oncomelania
formosana at different times and under different culture conditions (Experiment 3).
A. Plot showing growth after 4 months in the Plastic Trays.
B. Growth after an additional 2 months.
C. Approximately half of the above group was continued another 2 months (a total of 8
months) in a new tray.
D. The second half of the group was transferred and reared at 2 per Petri dish for an
additional 2 months, (total of 8 months in culture).
NUMBER OF SNAILS
GROWTH AND STUNTING IN ONCOMELANIA
4 months
6 months
8 months
Plastic Tray
8 months
Petri Dish
ES
о SC La OP AN AMEN Иа
LENGTH OF SHELL IN MM NUMBER OF WHORLS
93
94 VAN DER SCHALIE AND DAVIS
established in such a culture. All of
these young were derived from one
parental plastic tray culture. Since
at the end of 8 weeks little growth
was noted, the snails were maintained
in culture for an additional 8 weeks.
At the end of this period of 4 months
all of the snails were removed, meas-
ured, and their whorl counts determined.
Table 5 and Fig. 6A show that these
4-month-old snails were more stunted
than they would have been if they had
been placed in groups of 10 per Petri
dish (see Fig. 1). The mortality was
8% These snails were then returned
to their original tray and observed for
an additional 2 months when they were
again removed and measured. Another
6% of the snails had died and they
showed only little additional growth(Table
5, Fig. 6B).
After these 6 months of culture, the
snails were divided into 2 groups; 43
were placed in a new tray and returned
to culture under light (10-12 hours per
day) (Group A); 44 were placed in
Petri dishes, with 2 per dish, also
under light (10-12hours per day) (Group
B). At the end of 8 weeks (the animals
were then 8 months in culture) the snails
were removed from their cultures and
measured. The 43 snails of Group
A, in the trays, showed a 16% mortality.
Their average length was 3.0 mm and
the average whorl count was 5.0 (Table
5; Fig. 6C). The growth of these snails
was still less than. that of the snails
maintained in groups of 10 per Petri
dish for 8 weeks. No young were pro-
duced in the plastic tray culture over
the 8-month period. An analysis of
the gonads of 15 individuals of this group
revealed that all of them were in the
“undifferentiated” category (Table 4).
There was no mortality among the 44
snails of Group B, in the 22 Petri
dishes. Their average length was 5.8
mm and the average whorl count was
6.5 (Fig. 6D; Table 5). This growth
pattern was equal to that expected for
snails reared with 2 per dish for 8
weeks. An analysis of the gonads of
17 individuals in this group revealed
23% “undifferentiated,” 35% “almost
mature,” 23% “fully mature” (Table
4).
These results, when compared with
those of experiment 2B show a lag in
the development of some of those snails
which had been suppressed in growth
and development for 6 months. They
were slower in passing from an “un-
differentiated” gonadal condition to one
of “differentiation.” However, the same
magnitude of difference existed among
the “mature” or “almost mature” spec-
imens found in both experiments.
It is concluded that although the plastic
trays will maintain adult populations they
are not suitable for rearing young snails
which show extreme retardation and
mortality.
Analysis of Stunting and Whorl Count
In Oncomelania, the formation of a
varix on the shell occurs when the snails
have reached a length which can be
correlated with gonadal development in
the category of “mature” or “almost
mature.” The varix is a pronounced
thickening of the outer lip and after it
is formed little further growth occurs.
The following question now arose: is
it possible to examine a snail which
does not have a varix and determine
if it is stunted? In a number of non-
related experiments we had collected
records on the length of snails grown
under optimal conditions and the ac-
companying whorl counts. The number
of snails measured at each whorl stage,
along with the average length per whorl
count, is recorded in Table 6. The
average length per whorl countis plotted
and the standard deviation for the length
of shell at each whorl count is recorded
in. Fig, 1.
The whorls were counted to the nearest
half whorl by the following procedure.
The snail was held with the apex up
and with the outer lip to the right;
observations were made under a dissect-
ing microscope. The whorl count was
GROWTH AND STUNTING IN ONCOMELANIA 95
marked the final whorl.
Snails which had been stunted by
rearing in groups of 10 were used to
compare the average length per whorl
count with the normal condition as plot-
ted in Fig. 7 and Table 6. From this
comparison it can be seen that the num-
ber of whorls increases in a regular
manner when the snail is in an unfavor-
able environment, but the rate of shell
formation is decreased. In other words,
the size or height of each whorl is not
reduced in the stunted snail but the rate
of growth and speed of whorl formation
is greatly reduced compared with the
normal condition. It follows, therefore,
that one cannot determine the age of
a snail by its size alone. It is thus not
о 2 3 7 5 7 = = possible to differentiate a stunted snail
WHORLS from a snail grown under optimal con-
ditions, if both have the same size or
FIG. 7. The relationship between the length Whorl count. We find, in Oncomelania, as
THE STANDARD
DEVIATION FOR
THE LENGTH OF
EACH WHORL
(mm)
LENGTH OF SHELL IN MM
of the shell of Oncomelania formo- Ritchie et al. (1963) found for Australor-
sana and the whorl count for snails bis glabratus, that shell size is a more
grown under optimal conditions. important criterion for maturity thanage.
Development of Reproductive Organs in
then begun at the edge of the outer lip Relation to Size
and progressed up the shell. The posi-
tion of the tip of the apical whorl Both normal and stunted snails were
TABLE 6. The average length of shell per whorl count for normal and stunted Oncomelania
formosana snails
Stunted Snails
Whorls No. of snails Average No. of snails Average
measured length (mm) measured length (mm)
=~]
—
©
TAPP AAP Pwo ww py
O1 © O1 © 1 © O1 © 1 © 1 ©
D O1 # W & ND N M Hi © I
96 VAN DER SCHALIE AND DAVIS
TABLE 7. A comparison of degree of development of reproductive organs (lengths in mm)
among 5 stunted and 1 normal male and female Oncomelania formosana
8 months old 2 months old
(stunted) (normal)
d Specimen il 2 3 4 5 1
Shell 2.5 6.5
Gaia none 1
ne у found as
Prostate 0. 24 И
Verge 0. 22 3.4
? Specimen 1
Shell 6.5
Gonad 2.6
Accessory gland 5.7
— = not measured.
used to study the anatomy of the male
and female reproductive systems. We
found that stunting or suppression of
growth hindered the development of the
reproductive organs in a pronounced
manner. Many organs, such as the
gonad, prostate, verge, accessory gland,
spermathecal duct, bursa copulatrix,
etc., would not develop beyond their
rudimentary stages regardless of age
if the environment was such as to
retard growth. An example of this re-
tardation in development is shown in
Table 7 where 5 males and 5 females
were chosen as representatives of many
that were found to be similarly stunted.
These snails were taken fromthe plastic
tray culture of Experiment 3 when they
were 8 months old. The normal indi-
viduals were chosen at random from
Petri dishes where they had beenreared
2 per dish for 2 months.
In the stunted males the verge was
just a slight projection rising from the
“neck” region behind the tentacles;
the gonad was often undetected in gross
dissections. In females in their normal
state of growth the accessory gland is
a thick organ found along the full length
of the mantle cavity; it opens beside
the anus just posterior to the edge of
the mantle collar. In the stunted snails
this gland was only a slender thread
of tissue extending, in many cases, no
further than half way towards the mantle
collar from the rear of the mantle
cavity. The whole reproductive system
tends to remain undeveloped among the
animals thich have become stunted in
growth.
DISCUSSION
Culture Chambers.
The plastic tray culture in many
respects represents a small and sim-
plified aquaterrarium compared with that
described by Vogel (1948) and DeWitt
(1952); it is also similar to the culture
chamber used in the 406 Medical Gen-
eral Laboratory of the U. S. Army Gen-
eral Command, Japan (Moose, 1964).
Containers of this type which simulate
the natural environment have been used
for many years (see Sugiura, 1933).
The concept of using a Petri dish as
a simplified culture chamber is also not
new. Sandground and Moore (1955) used
GROWTH AND STUNTING IN ONCOMELANIA 97
10 cm and15 cm diameter Petri dishes;
they emphasized the difficulty in main-
taining and observing young snails in
a large tank-like aquaterrarium. Con-
sequently, they constructed an environ-
ment in their dishes resembling that
in their aquaterrarium, to provide a
sloping soil bank and a small reservoir
of water. For food they used strips
of filter paper impregnated with sodium
alginate. Komiya et al. (1959) used a
9 cm Petri dish as a “simple breeding
method for Oncomelania...” under vary-
ing conditions. They had a sloping
soil bank, which they described as good.
for adults, and a flattened soil mass
covered by a Sheet of water, which
they described as good for the young.
They recommended putting 8 to10adults
in such a container and 16-20 young
were not considered too many if they
were 3 mm or less in height. Cul-
tured diatoms and rice powder were
added for food.
It should be emphasized that rearing
young snails to maturity in the labora-
tory is a problem quite different from
that of maintaining adults and encour-
aging the production of young. Those
who previously recommended Petri dish
cultures failed to give any quantitative
data on the production of young, nor did
they give any rates of growth for young
snails. The problems relating to the
stunting of these snails were not recog-
nized so that the slow rates of growth
were generally taken for granted. The
Petri dish culture method described here
was tailored to meet the specific pro-
blems of rearing young snails to matur-
ity efficiently as well as in a predic-
table manner. One cannot rear large
numbers of young snailsinanaquaterra-
rium without inducing stunting.
Rates of Growth and Mortality
Table 8 was prepared to show the
rates of growth in Oncomelania for-
mosana, O. nosophora, and O. hupensis
obtained by various workers under both
field and laboratory conditions. The rates
of growth in this table were calculated
from the data presented by these authors
and are represented as rates converted
to mm per week. It is pertinent to
discuss how these rates were induced
as compared with conditions that were
found to stimulate optimal growth. Since
|TABLE 8. Comparison of growth rates for 3 species of Oncomelania, as reported in the
literature
Growth calculated] Laboratory |Laboratory|Calculated growth per week, in mm
light
condition
O.
hupensis
O. O.
formosana | nosophora
(field)
(field)
(field)
(field)
(field)
26
(field)
| Kojima 0.30
11962, Moose et al.
1965, van der Schalie
& Davis, this
paper
fluctuating
98 VAN DER SCHALIE AND DAVIS
O. nosophora, O. hupensis, andO. for-
mosana are allrelatively similarinsize,
their rates of growth under optimal
conditions in the laboratory were ob-
served to be about the same magnitude
during the first 8 weeks in culture.
This basic similarity enables us to
make some useful comparisons with the
data presented in Table 8.
We found that the growth of these
species of Oncomelania (starting at 0.5
mm length) under optimal conditions
follows a distinct sigmoid curve with
a reduction in growth rate at about
6.5 to 7 weeks. Calculations of change
in length per time beyond 8 weeks would
greatly reduce values of mm growth
per week. It is evident that, in 1933,
Sugiura provided an accurate estimate
of growth for O. nosophora in the field,
when the animals were in their logarith-
mic phase of growth; these data were
later confirmed by Hosaka et al.(1959).
The low rate obtained by McMullen
et al. (1951) under field conditions re-
sulted from measuring the change in
mode length when the initial measure-
ment involved snails already 4.0-5.0
mm long. Snails of this size are pass-
ing out of the ‘‘log phase’’ of growth
and the increase in length in mm per
week decreases markedly. Li (1953)
gave data which can likewise be accounted
for in this manner.
In the laboratory, it is now evident
that rates of growth of only 0.3-0.4
mm per week during the first weeks
of life indicate stunting and conditions
unsuitable for optimal growth. In the
data presented by the Laboratory (406)
Report (1962) crowding and the use of
room-level light probably accounts for
the low rates of growth (0.3-0.5 mm
per week). Komiya and Kojima (1961)
state that they reared their snails in
growth experiments under conditions
described by Komiya et al. (1959; dis-
cussed above under“Culture Chambers”).
They prescribed using room-level light
with the avoidance of direct sunlight.
They placed a single 2 mm Snail in
a 10 cm Petri dish. Temperatures varied
from 15°C to 25°C during their ex-
periments. These unusually low temp-
eratures and the use of room-level
light probably account for their low
growth rate (0.3mm). They gave no
mortality data. Komiya and Kojima
(1961) stated that Chi and Wagner (1957)
presented no temperature records and
that the latter data showed greater
growth than that obtained by themselves.
Actually, these authors reported that
they ran their experiments at 26°C
under constant light. Comparing the
curves for growth presented by Chi and
Wagner with those of Komiya and Kojima
during the first 8 weeks of culture,
the order of magnitude of growth in
mm per week was essentially the same:
about 0.3.
Chi and Wagner (1957) used constant
light from a 20 watt fluorescent (day-
light) tube 9-10inches above the cultures.
Newly hatched snails were reared at
26° C in a 7 ml pH beaker witha
small quantity of mud, a-piece of filter
paper, and some spring water. When
the snails reached 3.5 whorls they were
transferred to a 50 mm Petri dish
(1 per dish). They do not state whether
the mud was sterilized although in meth-
ods prescribed earlier by Wagner and
Wong (1956) the soil, sand, and gravel
were Sterilized. In spite of the pro-
vision of constant light and the 26°C
temperature they induced only a low
growth rate and they stated that the
growth rate “varied greatly between
snails of the same age.” The mor-
tality was 38%. The variance in growth,
low growth rate; and excessive mortal-
ity indicate an environment unsuitable
for the snails. The poor growth per-
haps could be attributed to sterile soil
and lack of a proper source of food
energy.
Mortality serves as an excellent cri-
terion for determining whether the lab-
oratory environment is optimal. In ex-
periment 1 our mortality rates were
24 and 36% for snails reared under con-
stant light; this high loss was cor-
related with an excessive algal condi-
GROWTH AND STUNTING IN ONCOMELANIA 99
tion. As shown in Table 2, by lowering
the amount of light, the excessive algal
condition was checked and mortality
dropped below 10% for snails reared
1 or 2 per dish. Our experience has
also shown that in the routine handling
of large numbers of young snails mor-
tality may increase due to mechanical
injury to the snails.
Overcrowding
Crowding also produces increased
mortality in addition to the stunting and
Suppression of sexual maturity. Large
culture chambers such as the plastic
trays become inefficient when only small
numbers of snails are reared in them,
so as to avoid stunting, because of
the necessity for active aeration, their
bulk, and increased maintenance. Like-
wise, the use of a small 5 cm Petri
dish proved unsuitable as a relatively
rapid algal growth and soil breakdown
lead to suppressed growth andincreased
mortality.
The interaction of the factors causing
stunting were not studied. Such a
study would involve a quantitative inves-
tigation of the relationships of food
supply, the effects of accumulated waste
material, and the effect of increased
physical interaction between snails ina
confined area.
We noted that increased mortality
for snails reared at higher densities
was due, in part, to an increased ten-
dency of young (2.5 whorls) snails to
climb up on the glass above the water
line. At that size they were inconspi-
cuous, were easily overlooked, and died
from desiccation. This behavior may
stem either from their avoidance of
accumulated waste or result from in-
creased snail interaction.
The increased tendency for crowded
Snails to climb from their culture cham-
ber is related to growth. Pesigan,
et al. (1958) found that O. quadrasi
continuously ingested food throughout
the 24-hour cycle so that the snails
changed gut contents every 3-10 hours.
We made a 24-hour study in the field
on the feeding of Pomatiopsis cincinna-
tiensis, a local species closely related
to Oncomelania. The North American
snails ate continuously and voided in
excess of 15 fecal peilets per hour
every hour. In crowded cultures the
climbing activity of the snails results
in a loss of energy to them as they
are moving or are dried to the sides
of the containers, not feeding. This
Significant loss of energy is possibly
the cause of reduced growth rates.
Conditions Favoring Optimal Growth
Optimal conditions for rapid growth
and development of Oncomelania are
based on the interaction and proper
balance of such factors as light, soil,
volume of the environment, and food
source. It is not yet possible here
to discuss quantitatively the many dif-
ferent interactions among these vari-
ables. Experimental evidence is needed
to explain how these several factors
combine to produce a favorable environ-
ment. If one considers light and the
volume of the culture as constant, then
soil and its accompanying microflora
are the critical variables. Excluding
the possible influence of trace elements
on growth, we find that a basic soil
of fine texture with a high calcium con-
tent, and capable of supporting a high
proliferation of diatoms is the most
suitable for culturing Oncomelania. It
is most important that decaying organic
material be present as well as the at-
tendant bacterial decomposers. Diatoms
in large numbers (such as the 10,000-
500,000 per gram of dried soil in the
river bank mud we used) provide a
constant turnover of decaying matter.
In Experiment 1, snails reared on
this soil and water in constant dark
grew at a rate of about 0.4 mm per
week. After 8 weeks in the dark the
soil was analyzed and was found to con-
tain sparsely scattered algal resting
cells and only a very few living diatoms.
These snails could survive and they did
grow on the organic material present
with its accompanying decomposing flora.
100 VAN DER SCHALIE AND DAVIS
In a previous study (Davis, 1962)
fecal pellets surgicallyiremoved from
the intestines of snailsf were; cultured
under optimal laboratory conditions.
Steriletechniques wereused in removing
the pellets. Many species of diatoms
and algae were cultured from this fecal
material. It is evident that many healthy
cells passed through the snail unaffected
by its digestive processes. These cir-
cumstances suggest that it is the weak-
ened, dying, and decaying cells provided
by a rich diatom flora which serve as
a source of energy for these snails.
Davis (1962) provided an experimental
model to determine if such a process
is operative in terms of energy flow.
Studies in the Medical General Lab-
oratory 406 (Report for 1955) also note
this voiding of undigested algal cells
(green and blue-green).
The positive value of diatoms as food
for Oncomelania in nature was indicated
by Mao (1958) and Komiya et al. (1959);
Stunkard (1946) also used diatoms as
a food additive in rearing snails. Dazo
and Moreno (1962) stated that O. quadrasi
“appears to be a herbivore; its diet
consists mainly of green algae and dia-
toms.” They also state that O. quadrasi
rarely ingested blue-green algae “al-
though these were abundant in the areas
studied.” The Medical General Lab-
oratory (406) reported (1955) that “as
a group the green algae appeared to
be more acceptable as food than the
blue-green algae.” They found that
some blue-green algae appeared to be
toxic for young snails; they did not
test diatoms.
ACKNOWLEDGEMENTS
Several technical assistants devoted
many hours of arduous work culturing
these Oncomelania, measuring them,
and gathering data used for this report.
For this assistance we are especially
indebted to: Berton Roffman, Robert
Wakefield and Andrew Bratton. The
program itself was sponsored by the
Commission on Parasitic Diseases (an
affiliate of the Armed Forces Epidem-
iological Board); their continued sup-
port has made these studies possible.
LITERATURE CITED
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1963, Investigations of a growth-
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CHERNIN, E. and MICHELSON, E. H.,
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, 1957b, Studies on the bio-
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CHI, L. W. and WAGNER, E. D., 1957,
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COLTON, H. S., 1908, Some effects
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DAVIS, G. M., 1962, A theoretical
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1962, Studies on the food and feed-
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1942, The effects of population den-
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283-289.
HOSAKA, Y., IJIMA, T., SASAKI, T.,
HASHIMOTA, I. and TSURUTA, J.,
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J. Parasit., 8: 745-748 (text in Jap-
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T., 1959, A simple rearing tech-
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MAO, C. P., 1958, Research on schis-
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MCMULLEN, D. B., KOMIYAMA, S.,
and ENDO-ITABASHI, E., 1951, Ob-
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of Schistosoma japonicum in Japan.
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MOOSE, J. W., WILLIAMS, J. E. and
FLESHMAN, P., 1962, Rice cereal
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V., 1955, Notes on the rearing of
Oncomelania spp. in the:laboratory.
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the United States. J. Parasit., 32:
539-552.
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VAN DER SCHALIE, H. and GETZ, L.
1962, Distribution and Natural History
of the snail Pomatiopsis cincinnati-
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68(1): 203-231. .
VOGEL, H., 1948, Uber eine Dauerzucht
von Oncomelania hupensis und Infek-
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Z. f. Parasitenkunde, 14: 70-91.
WAGNER, E. D. and WONG, L. W.,
1956, Some factors influencing egg
laying in Oncomelania nosophora and
Oncomelania quadrasi, intermediate
hosts of Schistosoma japonicum. Amer.
J. trop. Med. and Hyg., 5(3): 544-
558.
WRIGHT, C. A., 1960, The crowding
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of freshwater snails. Ann. trop.
Parasitol., 54: 224-232.
102
VAN DER SCHALIE AND DAVIS
RESUMEN
DESARROLLO NORMAL Y ARRESTADO EN
ONCOMELANIA (GASTROPODA, HYDROBIIDAE)
Se suministran datos concernientes al problema de la crianza de Oncomelania
en grandes cantidades, rapida, eficientemente y de una manera predictable, para
facilitar el estudio de Schistosoma japonicum en el laboratorio. Informacion pre-
via obtenida en otros laboratorios indica que la proporción de crecimiento
era de 0.3 - 0.4 mm por semana, en condiciones que producían gran mortalidad
38% en ciertos casos).
El procedimiento de cultivo aqui descripto, estimula un crecimiento uniforme
de unos 0.65 mm por semana con una proporción de mortalidad menor del 10%.
Crecimiento óptimo se obtiene cuando 1 o 2 caracoles recién nacidos (con 2 a 2.5
vueltas) se aislan en una cápsula de Petri de 9 cm. En el centro de la cápsula se
coloca una pequeña masa de tierra de textura fina sin estirilizar, que siendo al-
calina favorece el desarrollo de las diatomeas de su natural contenido. Se agrega
agua y la cápsula se cubre, ubicándola la luz de 150 bujías en ciclos de 10a 12
horas diarias. La temperatura debe mantenerse entre 25% + 20 C.; no se agrega
ningun alimento.
El aumento de individuos por cada cultivo a 5 y 10 produjo impedimentos en el
desarrollo, correlacionado con reducción en la madurez gonal, falta de desarrollo
en los organos sexuales, y mayor mortalidad. La concha de los caracoles asi
afectados no se distingue de la de los normales, y en consecuencia el individuo
retardado sólo puede identificarse si se conoce su edad.
El crecimiento óptimo depende de la interacción de los siguientes variables:
luz, adecuado volumen del recipiente, substrato en buenas condiciones y próspera
microflora. Cuando luz y volumen se mantienen constantes, un substrato rico en
calcio y capaz de mantener algas verdes en abundancia es un factor muy crítico.
|
MALACOLOGIA, 3(1): 103-110, 1965
FONTELICELLA (PROSOBRANCHIA: HYDROBIIDAE),
A NEW GENUS OF WEST AMERICAN FRESHWATER SNAILS!
WO: Gregg? and D. W. Taylor
Los Angeles, California, 0.5. A.
U. 5. Geological Survey
Menlo Park, California, U.S. A.
ABSTRACT
Fontelicella, g. п. , (subfamily Hydrobiinae) includes 3 subgenera: Fonteli-
cella s.s. (type F. californiensis, sp. n.), with 8 species, Pliocene to Recent,
of western U. S. A. and Baja California, México; Natricola, subg. п. (type
Pomatiopsis robusta Walker, 1908), with 3 species living in the Snake River
drainage of Idaho and Wyoming, U. S. A.; and Microamnicola, subg. n. (type
Amnicola micrococcus Pilsbry, 1893), with 1 species living in the Amargosa
River drainage of southern Nevada and southeastern California, U. S. A.
Among adequately described species, the most similar is Cincinnatia integra
(Say) of eastern U. S. A.; it differs in details of verge, radula, pigmentation,
shell, and foot. The described features of Fontelicella spp. include general
form, locomotion, behavior, pigmentation, external morphology, radula, verge,
eggs, and habitat. Arrangement of melanin and calcareous granules in the head
region is a particularly useful source of specific characters that has been
generally neglected in previous work on the family.
“ The generally small and characterless
shells of the Hydrobiidae have rarely
been sought by collectors in western
North America. There are even less
biological data available for this un-
popular group than in many others, so
from species to family rank their
classification is obscure. Our studies
have aimed at a partial survey of the
western American species, trying to
understand their histories and distri-
bution, and to fit the known fossil record
into a biological framework.
Preparation of a detailed, illustrated
account of the species will require
further work, but our observations so
far are comprehensive enough to permit
definition of a new genus. We publish
this paper to validate use of the names
in other papers in progress.
DIAGNOSIS
Family Hydrobiidae
Subfamily Hydrobiinae
Fontelicella 3 Gregg and Taylor, new
genus
Diagnosis. Shell 2.5-8 mm long in
adults, rimate or imperforate, narrowly
elongate to conic or globose, with
3-6 whorls, the aperture 20-40% of total
shell length. No sculpture except for
IContribution No. 4, Western American Freshwater Mollusks Program, Institute of Malacology.
“Research by Gregg was partially supported by National Science Foundation grant GB-1653.
3Latin fons, fontis, a spring; helix, helicis, a snail, and the feminine diminutive, -ella. Hence,
little spring snail. The name refers to a characteristic habitat of the group.
(103)
104 GREGG AND TAYLOR
minute growth striae. Embryonic shell
helicoid, umbilicate, with about 1 1/2
whorls. Verge bifid, with a narrow,
melanin-pigmented penis, and a usually
wider, virtually unpigmented, ductless
accessory process on the left. Ac-
cessory process usually with a terminal
glandular lobe, subterminal constriction,
and additional glandular areas in the
form of ridges, lobules or papules.
Radula - with formula 15 to 30: 17 to
24: 3 to 6-1-2 to 3: 3 to 7-1-3 to 7
1
from the second marginal to the central
tooth. Eggs laid singly in smooth,
unornamented capsules 0.3-0.5 mm in
diameter, either free in the substratum
or appressed to a firm surface.
Type. Fontelicella californiensis
Gregg and Taylor, new species.
Remarks. The names applied most
commonly to species here referred to
Fontelicella have been Paludestrina lon-
ginqua (Gould) and P. stearnsiana Pils-
bry. One of these two species might
therefore have been selected as type of
the genus. Amnicola longinqua is based
on fossil shells and may well be com-
posite. Although the living Paludestrina
stearnsiana is a recognizable Fonteli-
cella, no topotype material.can be col-
lected because the growth of Oakland and
other cities has destroyed the original
habitats. We consider F. stearnsiana a
valid species on the basis of near-
topotypes, but it is more prudent to
fix as type species one whose type
locality is likely to be available to future
students of the group.
The assignment of species described
from fossil shells (Amnicola longinqua,
А. micra, A. pilsbryana, and Hydrobia
truckeensis), and of the anatomically
unknown Paludestrina cedrosensis and
Pomatiopsis intermedia, to the genus is
based on shell characters only. Our
evaluation of these shell characters is
based on knowledge of the anatomy
of practically all described western
American Hydrobiidae as well as many
undescribed forms.
DESCRIPTION OF GENUS
Study of numerous species (in several
genera) of western American Hydrobi-
idae has revealed sets of characters that
unite the group we establish as Fonteli-
cella, and distinguish if from other
groups. The more conspicous characters
are listed in the generic diagnosis. Less
striking features that are commontothe
described and undescribed species we
have examined are summarized below.
General form, locomotion, behavior.
The elongate or globosely conic shell
2.5-8 mm long in adults is borne free
of the substratum, with the apex directed
upward and posteriorly to the right, so
that the axis of the shell forms an angle
of about 309-450 with the long axis of
the foot. In dorsal view when the snails
are crawling, the snout, tentacles, and
eyes are visible in front of the shell.
In different species or in different de-
grees of extension the broadly rounded
posterior end of the foot and the anter-
ior corners of the foot may also be visi-
ble. Compared to other Hydrobiidae we
have seen the snails crawl relatively rap-
idly; they move smoothly and do not show
the stepwise gait of the Pomatiopsinae.
The tentacles are relatively long and
slender, rod-shaped, tapering slightly or
imperceptibly to blunt tips, about 2/3-
3/4 as long as the shell aperture.
Cilia may occur in definite longitudinal
rows, or scattered with no obvious
arrangement. The tentacles are borne
diverging at an angle of 700-1000 (900
common), and usually are in vertical
or horizontal movement. They move
both above and below a plane parallel
with the substratum, and often touch the
substratum as if sensing it. We have
seen no rhythm in motion ofthe tentacles
in any species examined except F. hen-
dersoni, in which the tentacles move
up and down alternately.
In crawling the snail keeps its snout
appressed to the substratum and moves
it from side to side. This lateral
movement is inconspicuous when the
FONTELICELLA G.N. 105
snail is crawling rapidly, but when mov-
ing slowly and feeding the whole head
turns from side to side. In animals
with less heavily pigmented snouts the
action of the radula inside can be seen
as the animals browse.
Both direct observation of living snails,
and the worn radular teeth show that
the snails rasp food from a hard surface
as well as pick up fine particulate matter.
Field and laboratory observations, and
examination of fecal pellets, suggest that
the species of Fontelicella crudely select
detritus from soft mud or browse
microorganisms from the surface of
stones, dead wood, and decaying leaves.
When observed under a microscope,
specimens of Е. hendersoni showed a
positive tropism to the heat or light of
the lanp. No other species studied
showed this behavior, and it is probably
significant that F. hendersoni is the only
known Fontelicella of a warm spring
habitat.
Pigmentation. The externally visible
parts of the body are gray to deep
purple-black, from a variably dense
suffusion of fine melanin granules. No
other pigment is known in Fontelicella,
in contrast to Lithoglyphus, which has
both fine melanin granules and larger,
yellow-pigment granules. The other
elements of color in Fontelicella are
internal organs, ingested food, fecal
pellets, algal or other coating on the
outside of the shell, and abundant cal-
careous granules scattered through most
of the head-foot mass and concentrated
behind the eyes.
The pattern of pigmentation is speci-
fically diagnostic in nearly all species
of Fontelicella we have examined, and
there are even more marked differences
between the genera of Hydrobiidae. Our
work thus yields results similar to those
of Muus (1963), who found differences
in pattern between 3 Danish species of
Hydrobia. Although each colony of snails
may have considerable variability in the
density of melanin from one individual
to another, in nearly all species the
arrangement of melanin and calcareous
granules in the head region is distinc-
tive. Future work оп Hydrobiidae should
include critical attention to these fea-
tures as a source of taxonomic char-
acters.
The externally visible body of species
of Fontelicella varies in color from gray
to deep purple-black, but generally the
melanin is not uniformly diffused. The
dorsal and lateral aspects of the snout
and the operculigerous lobe are most
deeply pigmented, and ends and sides
of the foot, and ventral aspect of the
snout less pigmented. The tentacles
may be pigmented with diffuse melanin
granules like the head, or paler in
constrast, but lack discrete patches or
bands. When the tentacles are deeply
pigmented and bear a discrete ciliary
tract, the ciliated strip is outlined asa
less heavily pigmented area.
The eyes are set in swellings on the
outer bases of the tentacles, and appear
as intense black spots within a clear
area. A dense, conspicuous aggregation
of white granules adjacent to each eye
is characteristic of the genus. These
granulose areas often give the appear-
ance of eyebrows when they are narrow
regions immediately above and behind the
eyes. They also may be larger and more
diffuse, extending posteriorly on the
dorsum of the head, or they may lie
in front of the eyes on the lateral
aspect of the tentacles.
The sole of the foot in ventral and
lateral views can be seen to be unpig-
mented. When the upper surfaces of the
foot are deeply pigmented the color
change is abrupt, at a line running
around the edge of the foot just above
the sole. The lips are lightly pigmented
in contrast to the snout.
Pigmentation of the mantle, organs in
the mantle cavity, and upper head-foot
varies considerably from species to
species. The mantle may be opaque,
or so lightly pigmented that the stomach,
intestine, and outlines of the ctenidial
lamellae are visible. The density of
melanin decreases from the foot upward,
so that the body stalk and floor of the
106 GREGG AND TAYLOR
mantle cavity are virtually unpigmented.
The free portion of the penis is densely
suffused with melanin granules and is
in contrast to the light, unpigmented
accessory process.
Head-foot mass. The sole is about
2-3 times as long as wide when the
snail is crawling rapidly, but varies in
proportions with rate of travel. It
is broadly rounded at the hind end, with
parallel. sides, and widened by 2 auri-
culate lobes at the anterior corners.
The anterior border of the sole is straight
or slightly concave. An anterior pedal
groove traverses the anterior edge of
the foot; into this groove the anter-
ior mucus glands discharge their se-
cretions.
Scattered through the connective tissue
of the head-foot mass, mantle border,
and externally visible walls ofthe pallial
cavity are numerous relatively large
hyaline granules. These are visible only
where there is no dense epithelial suf-
fusion of melanin, and likely are spread
‘through all the head-foot mass, except
that they are rare in the tentacles.
The highly contractile snout is about
1/3 as wide as the foot, flattened-oval
in cross-section, and more convex dor-
sally. Ordinarily it is appressed to the
substratum in front of the foot, but the
anterior edge of the foot canbe stretched
farther forward than the end ofthe snout.
Two fleshy pads at the end of the snout
together form a roughly oval area in
anterior view, narrower dorsally. They
are divided in the median plane by the
slit of the mouth, and set off from the
more deeply colored snout by a narrow
constriction.
Mantle cavity. The mantle cavity has
the usual organization of hydrobiid snails.
From the roof of the cavity the ctenidium
hangs down as a Series of triangular
lamellae forming a ridge that divides the
cavity lengthwise into 2 approximately
equal parts. To the left on the mantle
lies the osphradium, and to the right
close to the junction of the roof and
floor of the cavity is the rectum. The
pallial oviduct lies between the rectum
and right side of the mantle cavity in
the female. The large verge fills much
of the cavity in the male.
Circulation in the mantle cavity is
simple, with a fairly strong inhal-
ant current on the left side and a
perceptibly weaker exhalant current out
of the right side. Ciliated epithelium
carries particles to be rejected from
the floor of the mantle cavity down
the right side of the body stalk to
the edge of the sole, along which they
are carried to the hind end of the
foot. This ciliated area has suffi-
cient force to carry a fecal pellet
up out of the mantle cavity and to
the rear of the foot when a snail is
held on its back. The exhalant current
is usually inadequate to this task. Cil-
iated epithelium on the left side also
carries particles down the body to the
edge of the sole and thence posterior-
ly.
The ctenidium consists ofabout 14-
30 triangular lamellae hanging down
from the mantle intothe mantle cavity.
It is nearly colorless and extends
from just inside the thickened mantle
border to the rear end of the mantle
cavity.
The fecal pellets are ovoidor spindle-
shaped, as in all Hydrobiidae seen, and
arranged lengthwise in the rectum. They
contrast with the cigar-shaped pellets
of Pleuroceridae that are arranged
transversely in all but the most distal
part of the rectum. Representative
measurements of the fecal pellets of
Fontelicella are .12 x .28 mm (ЕР.
hendersoni) and .11 x .25 mm (F. cali-
forniensis). They are composed of
vegetable fibres and tiny rock particles,
with no evident internal structure. The
pellets are voided singly as a rule, but
sometimes 2 pass through the anus
linked by a strand of mucus and fe-
cal material.
Verge. The verge is attached to
the floor of the mantle cavity, to the
right of the midline and behind the
right tentacle. It is relatively large
compared to other organs in the mantle
FONTELICELLA G.N.
cavity, and although directed for-
ward does not usually protrude from
the cavity. The forward direction
of the verge is in contrast to that
of some other genera, such as Lith-
oglyphus and Amnicola, in which the
verge curves to the left from its at-
tachment and extends through the me-
dian plane.
The relative size of the accessory
process and free portion of the penis
vary greatly. In Fontelicella stearnsi-
una the accessory process is about
1/4 as long, and slightly narrower than
the free penis. In Р. idahoensis it
is twice as long and about 6 times as
wide as the base of the free part of
the penis. Most species of Fontelicella
have an accessory process with compli-
cated ornament of small discrete glandu-
lar areas that appear as lowraised areas,
circular or elongate in plan, or as
secondary lobes that may reach nearly
the size of the rest of the accessory
process. The differences in pattern of
these glandular areas provide many of
the characters used in separation of
Species.
Radula. The odontophore bears about
55 (50 - 67 observed in adults) rows
of 7 teeth each. The central tooth is
approximately quadrilateral, about 2/3
as high as wide, and widest at the base
between the ventrolateral angles. The
reflection of the tooth is serrated into
a large, central, lanceolate cusp with
3-7 progressively smaller cuspsoneither
Side according to the species. The
strong basal ridge of the central tooth
has a strong basal denticle at its arch
on either side. The basal margin is
prolonged in the center into a tongue-
Shaped process extending about as far
as the ventrolateral angles. The pos-
terior surface of the tongue-shaped pro-
jection is concave, and successive teeth
interlock thereby.
The lateral tooth has a broad peduncle,
and 6-9 cusps on the reflection. The
longest and widest cusp is in the middle;
2-3 are medial and 3-6 lateral according
to the species, all becoming smaller
107
toward the sides. The base of the tooth
is bowed ventrally so that there is an
area convex ventrally, concave dorsally,
by which successive teeth of the lateral
series interlock. A ridge runsfrom this
ventrally concave projection to the dorsal
margin of the peduncle.
The first marginal tooth is falcate,
with a broad peduncle anda blade bearing
17-24 long, slender, sharp-pointed cusps.
A ventrally projecting ridge, concave
dorsally, extends nearly the whole length
of the peduncle and interlocks successive
first marginals.
The second marginal tooth is slightly
narrower, about as long as the first
marginal, but lacks an interlocking ridge.
The blade of the tooth is shorter, ser-
rated into 15-30 cusps that are shorter
and more slender than those of the first
marginal.
Operculum. The operculum is as in
most Hydrobiinae seen, corneous, pau-
cispiral, with a subcentral nucleus near-
er the basocolumellar edge.
COMPARISON
Cincinnatia is the only genus of ade-
quately described Hydrobiidae that shows
clear similarities to Fontelicella. Fea-
tures common to C. integra (Say) as
described by Berry (1943) and to species
of Fontelicella are a verge with one
duct (vas deferens), a relatively large
accessory process, and relatively small
penis. Differentia are shown in Table 1.
Subgenus Fontelicella s.s.,
new subgenus
Diagnosis. Shell small for the genus
(2.5-5 mm long, 3-4 whorls in adults).
Accessory process usually a little longer
than free penis. Habitat small springs,
seepages, or small streams, in soft
mud among dense aquatic plants, on
rocks or sticks. Eggs laid in capsules
usually free, or sometimes appressed to
substratum, usually difficult to see be-
cause of a coating of foreign matter.
Type. Fontelicella (s. s.) californiensis
108 GREGG AND TAYLOR
Fontelicella
imperforate or narrowly per-
forate
distinctly auriculate
most heavily pigmented part of
body.
TABLE 1
Shell distinctly umbilicate
Foot not auriculate
Snout lighter colored than head
Penis not heavily pigmented with
melanin
Accessory process
Central tooth
Lateral tooth
Gregg and Taylor, new species.
Distribution. Western United States
and northwestern Mexico, in the Great
Basin and Pacific drainages. California;
Nevada, southeastern Oregon, southeast-
ern Idaho, Utah, Arizona, and Baja
California. Known from rocks as old
as middle and perhaps early Pliocene.
This is the most widespread and speci-
ose group of west American Hydrobiidae.
Referred species.
Fontelicella (s. s.) californiensis Gregg
and Taylor, new species. Southern
California and northwestern Baja Cali-
fornia.
Fontelicella (s.s.) cedrosensis(Pilsbry),
1927 (Paludestrina). Cedros Island, Baja
California.
Fontelicella (s. s.) intermedia (Tryon),
1865 (Pomatiopsis). Owyhee River,
Malheur County, Oregon.
Fontelicella (s. Ss.) longingua (Gould),
1855 (Amnicola) in part. Subfossil, Col-
orado Desert, southern California.
Fontelicella (s. s.) micra (Yen), 1946
(Amnicola). Pliocene, Salt Lake Group,
Bear Lake County, Idaho.
Fontelicella (s. s.) pilsbryana (Baily and
a) with no terminal lobe set
off by subterminal
constriction
b) about 6 times width of
penis base
c) lacking glandular tissue
heavily pigmented with melanin
a) nearly always with terminal
lobe set off by subterminal
constriction
b) 2-6 (usually 2-3) times width
of penis base
c) with several discrete areas
of glandular tissue
3 to 7-1-3 to 7
1-1
2 or 3-1-3t0 6
Baily), 1952 (Amnicola). ¿Amnicola pils -
bryi Baily and Baily, 1951, non Walker,
1906). Bear Lake Valley, southeastern
Idaho-northeastern Utah.
Fontelicella (s.s.) stearnsiana (Pilsbry),
1899 (Paludestrina). San Francisco Bay
region eastward to Sierra Nevada foot-
hills, California.
Fontelicella (s. s.) truckeensis (Yen),
1950 (Hydrobia). Middle or early Plio-
cene, Truckee Formation, Churchill
County, Nevada.
Subgenus Natricola4
Gregg and Taylor, new subgenus
Diagnosis. Shell large for the genus
(4-8 mm long, 4-6 whorls in adults).
Accessory process about twice as long
as free penis. Habitat large springs,
rivers, or lakes, in mud or sandbottom,
on gravel, or onaquatic vegetation. Eggs
laid incapsules appressedto substratum.
* atin natrix, natricis, a water snake;-cola,
inhabitant. From the occurrence of most of
the species in the Snake River drainage.
FONTELICELLA G.N.
Type. Fontelicella (Natricola) robusta
(Walker), 1908.
Distribution. Snake River drainage
of western Wyoming and southern Idaho;
Harney Lake Basin, eastern Oregon.
Referred species.
Fontelicella (Natricola) hendersoni
(Pilsbry), 1933 (Amnicola), Harney lake
basin, Harney County, Oregon.
Fontelicella (Natricola) idahoensis
(Pilsbry), 1933 (Amnicola), Snake River,
southwestern Idaho.
Fontelicella (Natricola) robusta (Walk-
er), 1908 (Pomatiopsis), Jackson Lake,
Teton County, Wyoming.
Subgenus Microamnicola®
Gregg and Taylor, new subgenus
Diagnosis. Shell small for the genus
(1.5-1.7 mm long, 3 1/2 whorls in
adults), more nearly ovate. Accessory
process beyond fork of verge about
half as long as free penis, tapering to
a rounded distal end, lacking terminal
glandular lobe, subterminal constriction,
or other ornamentation. Free penis rod-
like, with parallel sides and rounded
distal end, heavily pigmented and visible
through shell and mantle. Habitat springs,
on rocks and aquatic vegetation. Eggs
laid in free capsules, less heavily coated
with adherent particles than in Fonteli-
cella s. s.
Type. Fontelicella (Microamnicola)
micrococcus (Pilsbry, in Stearns, 1893)
(Amnicola).
Distribution. Amargosa River drain-
age, in southern Nye County, Nevada;
eastern Inyo County, and northern San
Bernardino County, California.
Referred species. Only the type
Species is known in this subgenus.
Fontelicella (s. s.) californiensis®
Gregg and Taylor, n. sp.
Diagnosis. Shell about 3-4 mm long
5From the Greek word for small, and Amni-
cola.
6Named for the Californias, to which it is
restricted.
109
in adults, elongate-ovate, with 4 whorls.
Free part of penis moderately pigmented,
with a dorsal ridge extending nearly to
the tip. Accessory process about as long
as free part of penis, and about 3 times
as wide at the fork, with a terminal
lobe, subterminal constriction, and vari-
able ornamentation, usually including a
dorsal lobule, 1-5 dorsal longitudinal
ridges, and a ventral transverse ridge.
Main body of verge with a dorsal trans-
verse ridge that may unite with the dorsal
ridge on the accessory process or penis.
Type. University of Michigan Museum
of Zoology catalog number 220000.
Campo Creek, San Diego County, Cali-
fornia, 0.6 mi. east of Mountain Empire
Dam, W 1/2 SW 1/4 sec. 19, Т. 18 $., В.
5 ES. W. O. Gregg, W. В. Miller, 25-
III-1962.
Distribution. Southern California and
adjacent Baja California. From the
southern Sierra Nevada (on the western
slope only) through the western Trans-
verse Ranges and coastal plains to the
Laguna Mountains. This species is
characteristic of perennial springs and
small streams in the mountains. It
occurs in both the Pacific Ocean and
interior drainages.
REFERENCES
BAILY, J. L., JR. and BAILY, В. I,
1951, Further observations on the
Mollusca of the relict lakes in the
Great Basin. Nautilus, 65:46-53, 85-
93, Pl. 4.
and 1952, Amni-
~ cola pilsbryana, new name. Nautilus,
65: 144.
BERRY, E. G., 1943, The Amnicolidae
of Michigan; distribution, ecology, and
taxonomy. ‚Misc. Publ. Mus. Zool.
TLand in the United States is commonly di-
vided into “townships”, each6 miles square,
that are numbered according to tier (T.) and
range (R.) from standard base lines and
meridians. A township is divided into 36
“sections”, each section (sec.) 1 mile
square.
110 GREGG AND TAYLOR
Univ.Mich., 57: 1-68, Pl. 1-9.
GOULD, A. A., 1855, New species ofland
and fresh-water shells from western
(N.) America. Proc. Boston Soc. Nat.
Hist., 5:127-130.
MUUS, B. J., 1963, Some Danish Hydro-
biidae with the description of a new
species, Hydrobia neglecta. Proc.
malac. Soc. London, 35:131-138.
PILSBRY, H. A., 1899, Catalogue of the
Amnicolidae of the western United
States. Nautilus, 12:121-127.
1927, Expedition to Guadalupe
Island, Mexico, in 1922. Land and
freshwater mollusks. Proc. Calif.
Acad. Sci., ser 4, 16: 159-203, Pl. 6-
12.
1933, Amnicolidae from Wy-
oming and Oregon. Nautilus, 47:9-12,
Pl. 2, Fig. 1-10.
STEARNS, R. E. C.,
1893, Report on
the land and fresh-water shells col-
lected in California and Nevada by
the Death Valley Expedition, including
a few additional species obtained by
Dr. C. Hart Merriam and assistants
in parts of the southwestern United
States. N. Am. Fauna, 7:269-283.
TRYON, G. W., JR., 1865, Descriptions
of new species of Amnicola, Pomatiop-
sis, Somatogyrus, Gabbia, Hydrobia,
and Rissoa. Am. J. Conch., 1:219-
222, Pl. 22, Fig. 5-13.
WALKER, BRYANT, 1908, Pomatiopsis
robusta n. sp. Nautilus, 21:97.
YEN, T.-C., 1946, Late Tertiary fresh-
water mollusks from southeastern Id-
aho. J. Paleont., 20:485-494, Pl. 76.
1950, A molluscan fauna from
the type section of the Truckee For-
mation. Am. J. Sci., 248:180-193,
1 Pi,
RESUMEN
FONTELICELLA (PROSOBRANQUIA, HYDROBIIDAE)
UN NUEVO GENERO DE CARACOL FLUVIAL DEL OESTE AMERICANO
Fontelicella g. n. (subfam. Hydrobiinae) incluye 3 subgeneros: Fontelicella s.s.
(tipo F. californiensis sp. п.) con ocho especies del Plioceno al Reciente en el
oeste de Estados Unidos y Mexico (Baja California); Natricola subg. n. (tipo Po-
matiopsis robusta Walker, 1908) con tres especies en el sistema del Rio Snake
de Idaho y Wyoming; Microamnicola subg. n. (tipo Amnicola micrococcus Pilsbry,
1893) con su única especie viviente en el sistema del Rio amargosa del sur de
Nevada y sureste de California. Entre especies adecuadamente descriptas la mas
similar es Cincinnatia integra (Say) del oriente de Estados Unidos; difiere en
detalles de la verga, rädula y pigmentaciön, concha y pie. Los aspectos descriptos
de Fontelicella incluyen forma general, locomociön, comportamiento, pigmentaciön,
morfologia externa, radula, verga, huevos y habitat. El agrupamiento de granulos
de melanina y calcio en la region cefalica es de particular utilidad como caracter
especifico, y no habia sido tomado en cuenta en previos trabajos sobre esta familia.
MALACOLOGIA, 3(1): 111-181, 1965
ЗНДОПАРАЗИТИЧЕСКИЙ МОЛЛЮСК ASTEROPHILA JAPONICA
RANDALL ET HEATH (PROSOBRANCHIA: MELANELLIDAE)
И ЕГО СВЯЗЬ С ПАРАЗИТИЧЕСКИМИ БРЮХОНОГИМИ
Е. Н. Грузов
(Зоологический институт АН СССР)
Резюме
Строение эндопаразитического моллюска Asterophila japonica
Randall & Heath подверглось сильному изменению в процес-
се приспособления к образу жизни. Существующие сведения об
его анатомии во многом не верны, а его систематическое поло-
жение осталось невыясненным. |
Моллюск обитает в стенке тела ряда морских звезд /puc.1/,
распространенных вдоль азиатских берегов Тихого океана.
На поверхности женских особей прикрепляются карликовые нео-
‘гтенические самцы /рис. 3, 4 B/, строение которых до сего вре-
мени оставалось неисследованным.
В теле моллюска удается различить все основные отделы туло-
вища брюхоногих : голову, внутренностный мешок и ногу /рис.
6, 9/, олнако это деление сильно замаскировано.
Голова лишена щупалец и глаз. У самок она иногда вытянута,
в хобот /puc. 3, 14 A/, но чаще этот орган оказывается недо-
развитым /рис. 2/ или совсем исчезает /рис. 14 B/, у самцов
он всегда отсутствует /рис. 10/. За счет покровов головы
образуется прекрасно развитая ложная мантия /рис. 5(4),
рис. 6(1)/, целиком окружающая внутренностный мешок и ногу и
ограничивающая обширную псевдопаллиальную полость, в кото-
рой у самок происходит развитие яиц до стадии велигера.
Полость сообщается с внешней средой через отверстие на вен-
тральной стороне псевдопаллиума /рис. 2(3), рис. 5 (2)/.
Нога /рис. 6, 10, 22/ рудиментарна, лишена крышечки,
педальных желез и ползательной поверхности и не Ффункциони-
рует. К ноге мужских особей примыкает с правой стороны со-
вокупительный орган педального происхождения /рис. 9-10/.
У незрелых самцов иногда сохраняется рудимент передней пе-
дальной железы /puc. 24(8)/.
Внутренностный мешок /рис. 7-11/ утратил раковину и при-
обрел почти шаровидную форму, не сохранив следов спиральной
закрученности.
Мантия и мантийная полость рудиментарны, хотя сохранили
примитивное положение слева от ноги /рис. 6(8), рис. 9(3)/.
Мантийный комплекс органов распался и в большей части ре-
дуцировался. Только почка сохранила нормальное положение
и открывается в мантийную полость. Жабра, осфрадий, '"runo-
бранхиальная железа и ректум исчезли. Матка вынесена за
(111)
112
E. H. ГРУЗОВ
пределы полости /рис. 8(1)/ на правую сторону тела.
Пищеварительный аппарат начинается ротовым отверстием,
ведущим в мускулистую сосательную глотку, имеющую во фрон-
тальной плоскости два слепых выпячивания /рис. 14(12)/, ко-
торые Рандаль и Хиз (1912) считали рудиментами слюнных же-
лез. С другой стороны, можно считать их новообразованиями,
отсутствовавшими у анцестральных форм. Характерно, что
все представители Melanellidae - Entoconchidae, с которы-
ми А. japonica имеет много общего, лишены слюнных желез.
Вопрос о природе дивертикулов глотки Asterophila не может
‘быть решен окончательно, и поэтому то или иное толкование
этих образований не должно влиять на наше понимание систе-
матического положения исследуемой фофмы.
Недлинный, лишенный желез пищевод/рис. 25 (4)/ соединяет
глотку со слепо замкнутой пищеварительной железой - печенью
(2). Челюсти, радула, желудок и задняя кишка отсутствуют.
Кровеносная система тоже претерпела значительное вторич-
ное упрощение, касающееся главным образом сосудистого аппа-
рата. Перикардий сохранил нормальное положение на левой
стороне тела рядом с почкой /рис. 8(10), рис. 10(6)/.
Рено - перикардиальное отверстие отсутствует. Сердце дву-
камерное /рис. 8(8,9)/. Сосуды замещены системсй лакун и
синусов /рис. 12, 13/. Почка развита нормально. Респира-
ция происходит через поверхность псевдопаллиума..
Центральная нервная система имеет следующий план строе-
ния /рис. 31/. Церебральные и плевральные ганглии сливают-
ся друг с другом, образуя обширную ганглиозную массу (5,15),
лежащую над кишкой. Вентрально к ним примыкают два педаль-
ных ганглия (9), лежащих рядом с основанием ноги. Имеется
пара статоцистов (8). В глотке присутствуют два буккаль-
ных ганглия (1), соединяющиеся друг с другом двумя комис-
сурами (2). Висцеральное кольцо разомкнуто. Одна его по-
ловина состоит из висцерального (4) и субинтестинального(6) -
ганглиев, связанных с левой половиной церебро-плевральной
массы(15). Другая половина содержит единственный супраин-
тестинальный ганглий (12). Имеется хиастоневрия.
Головая система самок /рис. 38/ состоит из яичника и
выводных путей, дифференцированных в дистальной части на
3 отдела : дополнительную железу (4), семеприемник (3) u
матку (2). Склеенные в кокон яйца откладываются в полость
псевдопаллиума /рис. 6/.
Семенник /рис. 36(1)/ соединяется с семепроводом, обра-
зующим конечное расширение - дополнительную железу (6).
Личинка представляет собой типичного велигера с несколь-
ко редуцированным парусом /рис. 43-48/. В отличие от ли-
чинок Entoconchidae, она обладает перикардием и почкой.
Все строение Asterophila свидетельствует о ее близо-
сти к Melanellidae - Entoconchidae. так что выделение
ее в самостоятельное семейство Asterophilidae, как это
делает Thiele (1929), едва ли оправдано. Признаки для раз-
деления группы Melanellidae ua отдельные семейства,
Melanellidae, Stiliferidae, Pelseneeriidae и Paedophoropodidae)
A A A ee
ST
|
ASTEROPHILIA JAPONICA 113
также недостаточны. Правильнее объединять их в одно o6mNp-
ное семейство Melanellidae 5. lat., куда естественно
войдет и исследуемая Форма. Схема, представленная на рис.
49, иллюсгрирует Ффилогенетические взаимоотношения между
представителями данной группы.
1. Введение. Материал и методика.
Паразитизм среди брюхоногих моллюсков - явление сравнительно
редкое. В настоящее время известно. около 200 видов паразитиче-
ских Gastropoda при общем числе видов брюхоногих около 85000.
Тем не менее, изучение этих животных представляет большой обще-
биологический интерес, так как ни одна другая группа животных,
за исключением, может быть, ракообразных (Copepoda, Cirripedia)
не дает столь ясной картины процесса эволюции паразитов под
влиянием образа жизни.
Среди брюхоногих имеются все стадии перехода от свободно-
живущих Форм с высокой и совершенной организацией к глубоко спе-
циализированным и упрощенным эндопаразитам, представляющим собой
едва ли не самых деградированных представителей животного мира.
Подобный размах эволюционных изменений при наличии множества
переходных Форм позволяет изучить многие законрмерности и детали
процесса регрессивной эволюции. Отдельные представители парази-
тических Prosobranchia легко могут быть выстроены в ряд, иллю-
стрирующий этапы процесса приспособления животного к паразитизму.
Нирштрас (Nierstrasz, 1913), Ваней (Vaney, 1913), Иванов (1937a)
и др. показали, что подобный ряд весьма близок к филогенетическо-
му.
Много интересного дает также изучение адаптаций паразити-
ческих брюхоногих к конкретным условиям паразитирования, так как
в каждом отдельном случае ясны причины изменения тех или иных
органов.
Изучение паразитических моллюсков интересно и со стороны
их биологии, особенно биологии размножения. Увеличение количест-
ва продуцируемых яиц, забота о потомстве, ускорение индивидуально-
го развития, приспособления, обеспечивающие встречу самцов и са-
MOK, - таков далеко не полный перечень вопросов, поддающихся раз-
решению на данном материале.
Паразитизм среди Prosobranchia возникал по меньшей мере
5-6 раз в самых разнообразных семействах ; родственые связи этих
семейств со свободноживущими моллюсками в большинстве случаев ясны.
Имеется лишь несколько аберрантных форм с неясным систематическим
положением. Одной из таких форм до недавнего времени считалась
Asterophila japonica (Randall et Heath, 1912), изучению op-
ганизации которой и посвящена данная работа.
Сведения об этом своеобразном животном крайне скудны.
Моллюск был описан в 1912 г. Рандаль и Хизом (Randall et Heath, 1912).
Авторы приводят краткое описание женской особи Asterophila
(самцы остались им не u3BeCTHH) и ничего не сообщают о ее систе-
матическом положении.
114
BH TEYSOB
Нирштрас (Nierstrasz, 1913) ограничивается указанием Ha He-
возможность сближения этой формы е Ctenosculum и с другими па-
разитическими моллюсками.
Ваней (Vaney, 1914), напротив, сближает рассматриваемый
вид с Ctenosculum hawaiiense Heath, провизорно помещая
оба рода среди Aspidobranchia.
В 1929 году Тиле ( Thiele ) выделяет особое семейство
Asterophilidae, которое он относит к трибе Lamellariacea,
сближая, таким образом, Asterophila се Pseudosacculus и
Lamellariidae. Однако основания, которыми OH при этом руко-
водствовался, остались не ясными.
Наконец, в тридцатых годах исследование этого брюхоногого
предпринял А. В. Иванов, обнаруживший карликовых самцов этого ви-
да и собравший большой и интересный материал как по анатомии взро-
слых форм, так и по их эмбриональному развитию. Однако это иссле-
дование не было доведено до конца, и в печати появились только
отрывочные сведения, разбросанные по различным работам (Иванов,
1937 a, 1944 1945, 91952 m Ир.)
Таким образом, к настоящему моменту большинство фактических
сведений о строении Asterophila практически попрежнему нахо-
дятся в небольшой работе Рандаль и Хиза, которая основана на изу-
чении всего лишь шести женских особей. Естественно, что авторы
не смогли избегнуть ряда ошибок, и наши знания об анатомии и о
систематическом положении А. japonica в настоящее время совер-
шенно недостаточны.
Между тем, исследование этого интересного брюхоногого, под-
вергшегося сильному изменению в процессе приспособления к пара-
зитическому образу жизни, может расширить наши представления не
только об его эволюции, но и о морфологических закономерностях
эволюции других паразитических гастропод.
Учитывая это, проф. А. В. Иванов передал в мое распоряжение
все свои матерыалы по Asterophila, содержащие множество фикси-
рованных животных, препараты и рисунки, и положил начало данному
исследованию. В течение всей работы я много раз пользовался его
советами и теперь рад случаю принести ему мою искреннюю благо-
дарность.
Всего в моем распоряжении имелось около 600 женских особей
Asterophila, что позволило судить He только о нормальной aHa-
томии животного, но и о наиболее характерных отклонениях в его
строении. На многих особях находились прикрепленные карликовые
самцы этого вида, организация которых до сего времени оставалась
неизвестной. В ложномантийной полости половозрелых самок при-
сутствовали личинки на разных стадиях развития.
Моллюски были зафиксированы самыми разнообразными Ффиксато-
рами : жидкостью Ценкера, сулемой с уксусной кислотой, жидкостью
Флемминга, пикриновой кислотой (по Буэну) и др. Сравнительно
крупные (до 35мм) размеры животного позволили значительную часть
анатомии женских особей исследовать путем вскрытия. Полученные
таким образом сведения всегда проверялись и дополнялись при изу-
чении серий срезов. Заливка в парафин производилась через н.-бу-
тиловый спирт. Срезы окрашивались железным гематоксилином Гей-
денгайна с подкрашиванием лихтгрюном и бисмаркбрауном, а также
по Маллори и азокармином по Гейденгайну. Последний способ давал
ASTEROPHILA JAPONICA 115
наиболее четкие картины. Для выявления слизистых клеток применяласт
окраска. тионинсм и толуидинблау.
Строение животного восстанавливалось по срезам методом графи-
ческих реконструкций. В отдельных случаях, когда это оказывалось
необходимым, приходилось прибегать к объемным пластическим
реконструкциям.
В результате исследования строения Asterophila я пришел к
выводу о ее принадлежности к группе моллюсков, связанных с
Melanellidae. Поэтому при сопоставлении нашей формы с другими
паразитическими моллюсками, упор делается на сравнении с предста-
вителями Melanellidae, Stiliferidae, Entoconchidae и -Paedo-
phoropodidae.
2. Распространение Asterophila и ee хозяева.
Географический ареал А. japonica чрезвычайно широк.
Моллюск встречается вдоль всего азиатского побережья северной
части Тихого океана от Берингова пролива до Кореи на глубинах от
14 до 700 метров. Вполне вероятно, что действительные границы
его ареала еще шире.
Такое распространение паразита в значительной степени объяс-
няется его малой специфичностью : хозяева Asterophila находятся
среди всех отрядов Asteroidea: Phanerozonia, Spinulosa и
Forcipulata. Подавляющее большинство особей было добыто из
Ctenodiscus crispatus Retzius, и Leptasterias polaris Müller
et Troschel. Кроме того, моллюски попадались в Leptychaster Sp.,
Cribrella sp., Leptasterias groenlandica (Lütken) и Г. arctica (Murdoch).
Зараженные звезды обычно легко узнаются по внешнему виду,
т. к. моллюски вызывают деформацию стенки тела хозяина.
Моллюск находится между соединительной тканью стенки тела
звезды и перитонеальным эпителием, выстилающим целомическую по-
лость /рис. 1/. Перитонеум над моллюском немного растянут и плот-
Разрез через луч
звезды. Схема.
1 - стенка тела; 2-
полость луча; 3 -
перитонеальный эпите-
лий звезды; 4 - плас-
тинки амбулакрального
скелета; 5 - пластин-
ки адамбулакрального
скелета.
Location of male and female Astero-
phila japonica in the host. Section
through ray of starfish. Diagram-
matic. 1- body wall; 2- cavity of
Puc. 1. Положение самца и ray; 3 - peritoneal epithelium of
FIG. 1. самки Asterophila starfish; 4 - plates of ambulacral
japonica в хозяине. skeleton; 5 - plates of adambulacral
skeleton.
116
EH. ГРУЗОВ
HO прилегает к его ложной мантии. Скелетные элементы участка ко-
жи, с которым соприкасается моллюск, сильно деформированы. Стен-
ка тела в этом месте образует чашевидное углубление, снаружи вы-
ступающее в виде опухоли. Y Leptasterias на дне yr-
лубления, в одной из ячеек между скелетными пластинками, заметно
очень маленькое сморщенное отверстие, прободающее стенку луча.
Моллюск внутри опухоли располагается так, что отверстие в его
ложной мантии (наружное половое отверстие) лежит против отверстия
в стенке луча и его псевдопаллиальная полость сообщается, таким
образом, с внешней средой. У остальных исследованных звезд от-
верстие в стенке тела отсутствует, но слой кожи между пластинка-
ми скелета бывает чрезвычайно тонким. По всей вероятности, связь
паразита с наружной средой, необходимая для выведения.наружу ли-
чинок, осуществляется периодически через разрыв истонченного уча-
стка кожи, который позднее регенерирует.
На дне чашевидного углубления стенки тела морской звезды
обычно наблюдается углубление, меньших размеров, в котором поме-
щается карликовый самец Asterophila. Самцы встречаются только
вместезс самками и сидят на их ложной мантии недалеко от Hapyx-
ного полового отверстия. Отверстие в псевдопаллиуме самцов об-
ращено к женскому половому отверстию. В тех случаях, когда на
самке находится несколько мужских особей Asterophila, под каждой
из них стенка тела морской звезды образует небольшие дополнитель-
ные углубления.
Ротовое отверстие самок А. japonica обращено к стенке тела,
хозяина, рот мужских особей обычно погружен в ложную мантию са-
мок.
Интересно сравнение положения Asterophila внутри хозяина
а таковым других паразитических брюхоногих.
В семействе Melanellidae наблюдается постепенный переход
от форм, паразитирующих на поверхности тела иглокожих,к настоя--
щим эндопаразитам. Первый шаг к глубокому погружению в Cutis
хозина делает Megadenus arrhynchus Ivanov, живущий в глубине
цистообразного углубления стенки тела морской звезды Anthenoides
rugulosus Fisher. Животное Целиком находится внутри цисты,
однако его связь с внешней средой еще велика, т. к. циста широко
открыта наружу. Ротовое отверстие Megadenus обращено к стенке
тела звезды (Иванов, 1952).
Bee представители рода Stilifer живут в толще стенок тела
хозяина и сообщаются с наружной средой только узким отверстием
ложномантийной полости. Хобот этих форм прободает стенку тела и
проникает в целомическую полость (P. and Е. Sarasin, 1885; Hirase,
1932; Иванов, 1952 и др.).
Наиболее измененный представитель семейства, Gasterosiphon
deimatis (Koehler et Vaney) оказывается уже истинным эндопара-
зитом. Как сообщают Келер и Ваней ( Koehler et Vaney, 1903), он
обитает в полости тела голотурии Deima blakei Theel, прикреп-
ляясь хоботом к маргинальному сосуду на кишке хозяина. Связь па-
разита с внешней средой поддерживается посредством сифона, откры-
вающегося через стенку тела голотурии.
Все Ещосопсшаае - настоящие эндопаразиты, обитающие в
полости тела различных голотурий, однако способ их прикрепления
eee eee TE ee ee
ASTEROPHILA JAPONICA 117
несколько варьирует. ÆEntocolax ludwigi Voigt, E. schiemenzi
Voigt, E. trochodotae Heding и Етосопсйа mirabilis Braun
прикрепляются при помощи сифона к стенке тела голотурии ( Voigt,
1888, 1901; Heding, 1934; Müller, 1852). Остальные вилы
Entocolax, a также Enteroxenos и Parenteroxenosl по данным
Шванвича (Schwanwitsch, 1917), Бонневи ( Bonnevie, 1902) и
‘Иванова (1945, 1947), прикрепляются к кишке голотупий. Тело
Enteroxenos и Parentevoxenos одето перитонеальным эпителием
хозяина, отходящим от его кишечника ( Bonnevie, 1902; Иванов,
1947).
По способу паразитирования Asterophila занимает mpomexy-
точное положение между Stiliferidae и Entoconchidae.
Подобно Megadenus arrhynchus, живущему Ha дне чашеобразного
углубления стенки тела звезды, ее ротовое отверстие обращено к
стенке тела хозяина, откуда моллюск добывает свою пищу. Однако
в отличие от всех Stiliferidae (за исключением Gasterosiphon),
Asterophila прошла сквозь толщу стенки тела звезды и обитает
под перитонеальным эпителием. Подобно примитивным Entoconchidae
она сохраняет связь с внешней средой через стенку тела хозяина.
3. Организация взрослых животных
1. Внешний вид
Рандаль и Хиз приводят удачное описание внешности типичной
самки Asterophila, хотя, имея дело всего с шестью особями, они,
естественно, не смогли коснуться вопроса об индивидуальной измен-
чивости животных, которая очень велика.
Паразитизм наложил на А. japonica глубокий отпечаток, в ре-
зультате чего моллюск совершенно утратил облик переднежаберной
улитки. Снаружи все тело животного одето ложной мантией, так что
при внешнем осмотре животного. видны лишь этот орган и хобот.
Часто сквозь тонкие стенки псевдопаллиума просвечивают внутрен-
ностный мешок и яйцевой кокон.
Рис. 2 передает внешность неполовозрелой самки, ее ложная
мантия (1) не растянута и шаровидна. Животное изображено с брюш-
ной стороны, которая легко узнается по находящемуся на ней вторич-
ному половому отверстию (3). У особей, достигпих половой
зрелости, вокруг отверстия сидят самцы /puc.3/.
Ложная мантия лишена опорных образоваий и легко растягивается
и деформируется, что сильно меняет облик животного. Большинство
экземпляров имеют бобовидную форму /рис. 4, 5/; иногда приобре-
тают вид гантели, или деформированы в еще большей степени.
Внешний вид самцов гораздо более постоянный, чем у самок.
По-видимому, нормой и здесь следует признать сферическую Форму те-
ла, хотя часто встречаются и экземпляры, имеющие овальные очерта-
e lle rindo OIR AIR O RN а Pe a
ae (Baer, 1952) предлагает считать Parenteroxenos Ivanov
синонимом Thyonicola Mandahl-Barth. Однако описание Мандаль-
Барта, ( Mandahl-Barth, 1941) так неполно, что объединять эти
формы в настоящий момент преждевременно.
118
Be GH. SEEYSOB
PUC
ICI
Рис. 2.
FIG. 2,
Asterophila japonica.
Aslerophila japonica.
Внешний вид неполовозре-
лой самки.
1 - ложная мантия; 2 -
внутренностный мешок; 3 -
отверстие ложной мантии;
4 - ротовое отверстие; 5-
хобот.
Ventral view
of immature female. 1 - pseudopal-
lium;
2 - visceral mass; 3 - open-
ing ofpseudopallialcavity; 4 - open-
ing of mouth; 5 - snout.
=
Asterophila japonica.
Самка и самцы, прикрепив-
шиеся вокруг отверстия
ложной мантии.
Asterophila japonica. Female, and
males clustering around the opening
of the pseudopallial cavity of the fe-
male.
ASTEROPHILA JAPONICA 119
2 тт
B
Puc. 4. Asterophila japonica. Половозрелая самка. A - Вид co
FIG. 4. спинной стороны. Б - Вид с брюшной стороны.
1 - внутренностный мешок; 2 - хобот; 3 - ротовое отверстие;
4 - яйцевой кокон; 5 - отверстие ложной мантии.
Asterophila japonica. Mature female. A, dorsal view; В, ventral view. 1- visceral
mass; 2-snout; 3- opening of mouth; 4- cocoon-like egg mass; 5 - opening of
pseudopallial cavity.
120 E. H. ГРУЗОВ
ния /рис. 3, 5/. Сквозь стенки псевдопаллиума самцов просвечивает
внутренностный мешок и совокупительный орган, который иногда высо-
вывается наружу через отверстие ложной мантии /рис. 5/.
Рис. 5.Asterophila japonica Y,
FIG. 5.Вид с левой стороны (ри-
сунок А. В. Иванова).
1 - пенис; 2 - отверстие
ложной мантии; 3 - внут-
ренностный мешок; 4 - лож-
ная мантия.
Asterophila japonica d. View from
left side (after A. V. Ivanov). 1-
penis; 2- opening of pseudopallial
cavity; 3- visceral mass; 4 -
0 -5mm pseudopallium.
Дополнительной причиной изменчивости внешнего вида моллюска,
служит хобот. Большинство особей обладают хоботом, к которому хо-
рошо подходит название, данное Рандаль и Хизом:"ротовая папилла".
Это невысокий бугорок, закругленный у вершины, где помещается ро-
товое отверстие. Иногда, особенно у самцов, он совершенно пропа-
лает, иногда же, напротив, приобретает вид массивного цилиндричес-
кого образования /рис. 14, A.
Размеры тела колеблются в зависимости от возраста в пределах
от 2 до 35 мм; диаметр внутренностного мешка не превосходит 15мм.
Самцы редко бывают более 2мм. Тело моллюска, по сообщению А. В.
Иванова, желтовато-белого цвета.
После удаления ложной мантии /рис. 6-11/ становятся заметны
внутренностный мешок животного и рудимент ноги, помещающийся у его
основания против отверстия псевдопаллиума. К ноге самцов прилега-
ет развитый penis /рис. 10 (9)/. Присутствие ноги помогает ус-
тановить правильную морфологическую ориентировку тела Asterophila:
плоскость, проходящая через ротовое отверстие, вершину внутренност-
ного мешка и середину ноги, представляет собой медиальную плоскость,
ротовое отверстие находится на переднем конце тела, а нога распо-
лагается на брюшной стороне. Подобная ориентировка полностью сов-
падает с той, которая была принята Рандаль и Хизом.
Внутренностный мешок, лишенный раковины и спиральной закру-
ченности, как у самцов, так и у самок имеет шаровидную' Форму и
обычно слегка сплюснут с боков или в дорзо-вентральном
направлении. Спереди он срастается с основанием псевдопаллиума
Ha передней стороне внутренностного мешка слева от ноги тянется
Узкая складка мантии /рис.7 (4) и рис. 9 (3)/. Около ее левого
края сквозь покровы тела просвечивает перикардий /рис. 8 (10)/ и
почка /рис. 8 (7)/. На правой и брюшной поверхности внутренност-
ного мешка заметны выводные пути половой системы. У самок /puc.8/
это белковая железа (5), семеприемник (2) и матка (1); у самцов
/рис. 9/ - семепровод и дополнительная железа (1). И женское, и
ASTEROPHILA JAPONICA 121
Puc. 6. Asterophila japonica Y.
FIG. 6. Ложная мантия вскрыта.
Вид с брюшной стороны.
1 -- ложная мантия; 2 -
яйцевой кокон; 3 - яичник;
4 - печень; 5 - нога; 6 -
Asterophila japonica?. Pseudopal-
lium opened. Ventral view. 1-
pseudopallium; 2 - cocoon-like egg
mass; 3-ovary; 4-liver; 5-
отверстие ложной мантии; foot; 6 - opening of pseudopallial
7 - хобот; 8 - мантия; 9 - cavity; 7- snout; 8- mantle; 9-
перикардий; 10 - сердце. pericardium; 10 - heart.
Рис. 7. Aslerophila japonica Y.
FIG. 7. Ложная мантия удалена. Вид
со спинной стороны.
1 - яичник; 2 - печень;
3 - белковая железа; 4 -
Asterophila japonica 2. Pseudopal-
lium removed. Dorsal view. 1-
ovary; 2 - liver; 3 - albumen gland;
мантия; 5 - ложная мантия; 4- mantle; 5 - pseudopallium; 6 -
6 - ротовое отверстие; 7 - opening of mouth; 7- snout; 8 -
хобот; 8 - семеприемник; seminal receptacle; 9 - pallial ovi-
9 - MaTKa. duct.
122
Prc.
ESPE: REYIOD
—
8. Asterophila japonica $.
FIG. 8. Ложная мантия удалена.
Вид спереди.
1 - матка; 2 - семеприем-
ник; 3 - яичник; 4 - пе-
чень; 5 - белковая железа;
6 - хобот; 7 - почка; 8 -
предсердие; 9 - желудочек;
10 - перикардий; 11 - ро-
товое отверстие; 12 - пе-
редняя лопасть ноги; 13 -
задняя допасть ноги; 14 -
ложная мантия; 15 - половое
отверстие.
Asterophila japonica Y. Pseudopal-
lium removed. Anterior view. 1-
uterus; 2 - seminal receptacle; 3 -
ovary; 4- liver; 5 - albumen gland;
6 - snout; 7- kidney; 8 - auricle;
9 - ventricle; 10 - pericardium;
11 - opening of mouth; 12 - anterior
part of foot; 13 - posterior part of
foot; 14 - pseudopallium; 15 - gen-
ital opening.
mm
Рис. 9. Asterophila japonica Y.
FIG. 9. Ложная мантия удалена.
Вид спереди.
1 - дополнительная железа;
2 - половое отверстие; 3 -
мантия; 4 - сердце; 5 -
перикардий; 6 - ротовое
отверстие; 7 - нога; 8 -
ложная мантия; 9 - пенис.
Asterophila japonica $. Pseudopal-
lium removed. Anterior view. 1-
accessory gland; 2- genital open-
ing; 3- mantle; 4 - heart; 5 - per-
icardium; 6 - opening of mouth; 7 -
foot; 8 - pseudopallium; 9 - penis.
ASTEROPHILA JAPONICA 123
Рис. 10. Asterophila japonica Y.
FIG. 10. Ложная мантия удалена.
Вид с левой стороны.
Asterophila japonica d. Pseudopal-
1 - внутренностный мешок;
lium removed. View from left
2 - пенис; 3 - нога; 4 - side. 1 - visceral mass; 2 - penis;
ложная мантия; 5 - мантия; 3 - foot; 4 - pseudopallium; 5-
6 - перикардий. mantle; 6 - pericardium.
Puc. 11. Asterophila japonica с’.
FIG. 11. Ложная мантия удалена.
Вид с правой стороны.
1 = пенис; 2 - внутренно-
стный мешок; 3 - дополни-
тельная железа; 4 - ман-
тия; 5 - ложная мантия;
6 - ресничная борозда.
Asterophila japonica 9. Pseudo-
pallium removed. View from right
side. 1 - penis; 2 - visceral mass;
3- accessory gland; 4- mantle;
5 - pseudopallium; 6 - ciliated
neHuca. groove of penis.
124 Е. H. ГРУЗОВ
Рис. 12. Общий план строения самца ресничная борозда пениса;
FIG. 12. Asterophila japonica. Схема. 24 - ложная мантия; 25 -
1 - семенник; 2 - семе- кровеносные лакуны.
провод; 3 - дополнитель-
ная железа; 4 - крове-
HOCHM синус; 5 - виесце- Gross anatomy of male Asterophila
ральный ганглий; 6 - поч- japonica. Diagrammatic. 1 - tes-
ка; 7 - половое отверстие; tis; 2- уаз deferens; 3- acces-
sory gland; 4- blood sinus; 5-
visceral ganglion; 6 - kidney; 7 -
genital opening; 8- mantle; 9-
subintestinal ganglion; 10 - cepha-
lic blood sinus; 11 - cerebro-pleu-
ral ganglionic mass; 12 - esopha-
gus; 13- buccal ganglion; 14-
pharynx; 15 - pharyngeal diverti-
8 - мантия; 9 - субинтес-
тинальный ганглий; 10 -
головной кровеносный си-
Hyc; 11 - церебро-плев-
ральная ганглиозная мас-
са; 12 - пищевод; 13 -
буккальный ганглий; 14 -
глотка; 15 - дивертикулы culum; 16 - pedal ganglion; 17-
глотки; 16 - педальный supraintestinal ganglion; 18 - per-
ганглий; 17 - супраинтес- icardium; 19- foot; 20 - liver;
тинальный ганглий; 18 - 21 - opening of pseudopallial cavi-
перикардий; 19 - Hora; ty; 22 - ciliated groove of penis;
20 - печень; 21 - отвер- 23- penis; 24 - pseudopallium;
стие ложной мантии; 22 - 25 - blood lacunae.
мужское половые отверстия имеют вид узкой и длинной щели, распола-
гающейся справа от ноги /рис. 8 (15); рис. 9 (2)/. В экваториаль-
ной части внутренностного мешка находится печень /puc.?7 RATE
а вершину занимает ToHana. У женских особей граница между этими
органами хорошо заметна снаружи, благодаря тому, что яичник,
наполненный яйцами с большим количеством желтка, выделяется своим
цветом, а сквозь тонкие стенки печени просвечивают ее многочисленные
внутренние складки.
Наиболее существенными особенностями наружного строения
Asterophila нужно признать следующие: 1) отсутствие раковины
Рис.
ASTEROPHIA JAPONICA
13. Общий план строения сам-
FIG. 13. ки Asterophila japonica.
Cxema.
1 - яичник; 2 - эпителий
внутренностного мешка; 3 -
кровеносный синус; 4 -
кровеносные лакуны; 5 -
яйцевод; 6 - печень; 7 -
висцеральный ганглий; 8-
белковая железа; 9 - поч-
ка; 10 - мантия; 11 - суб-
интестинальный ганглий;
12 - церебро-плевральная
ганглиозная масса; 13 -
пищевод; 14 - глотка; ‘15 -
буккальный ганглий; 16 -
дивертикулы глотки; 17 -
ротовое отверстие; 18 -
головной кровеносный си-
нус; 19 - педальный ганг-
лий; 20 - супраинтести-
нальный ганглий; 21 - пе-
рикардий; 22 - нога; 23 -
отверстие ложной мантии;
24 - самец; 25 - половое
отверстие; 26 - матка;
27 - семеприемник; 28 -
ложная мантия; 29 - яй-
цевой кокон.
Gross anatomy of female Astero-
phila japonica. Diagrammatic. 1-
ovary; 2- epithelium of visceral
mass; 3- blood sinus; 4 - blood
lacunae; 5 - oviduct; 6 - liver; 7 -
visceral ganglion; 8 - albumen
gland; 9 - kidney; 10 - mantle;
11 - subintestinal ganglion; 12 -
cerebro-pleural ganglionic mass;
13 - esophagus; 14 - pharynx; 17 -
opening of mouth; 18 - cephalic
blood sinus; 19 - pedal ganglion;
20 - supraintestinal ganglion; 21 -
pericardium; 22 - foot; 23 - open-
ing of pseudopallial cavity; 24-a
male; 25 - genital opening; 26 -
pallial oviduct; 27 - seminal re-
ceptacle; 28 - pseudopallium; 29 -
cocoon-like egg mass.
и спиральной закрученности внутренностного мешка, 2) сильную pe-
дукцию головного отдела, ноги и органов мантийного комплекса и
3) развитие псевдопаллиума..
Все эти признаки указывают на глу-
125
126 Her ISMTPYSOB
pS
OD
©
N
ur
3
3
|
Las
лий;
7 - покровный эпите-
oe
кольцевые Мышцы;
9 - продольные мышцы;
соединительная ткань;
10 -
114
глотка? Ter =
глотки; 13 - ротовое от-
верстие; 14 - пищевод;
15 - ганглии центральной
нервной системы.
дивертикулы
Asterophila japonica Y. Frontal
sections through anterior end of
body. Diagrammatic. A - snout
developed; В - snout absent. 1-
liver; 2- pericardium; 3 - heart;
4- pseudopallium; 5 - cephalic
Asterophila japonica 2.
Фронтальный разрез через
передний конец тела.
Схема. A - особь с раз- blood sinus; 6- blood sinus of snout;
витым хоботом; Б - особь, 7 - surficial epithelium; 8 - trans-
лишенная хобота. verse muscle; 9 - longitudinal mus-
1 - печень; 2 - перикар- cle; 10- connective tissue; 11-
дий; 3 - сердце; 4 - лож- pharynx; 12- pharyngeal diverticu-
ная мантия; 5 - головной lum; 13- opening of mouth; 14-
кровеносный синус; 6 - esophagus; 15 - ganglion of cen-
кровеносный синус хобо- tral nervous system.
бокую перестройку организации B связи с далеко зашедшим
соблением к паразитизму.
Отсутствие раковины и связанная с этим деспирализация внут-
ренностного мешка сближает нашу форму с паразитическими Ento-
conchidae и Paedophoropodidae. Bee Melanellidae и Stiliferidae
приспо-
ASTEROPHILA JAPONICA 127
обладают высокой закрученной раковиной D)?
ASEO OO E
Хобот, как указывалось, очень мал и часто совсем не выражен.
В наиболее развитом виде он имеет форму закругленного у вершины
цилиндра. Его строение видно на продольном срезе, представленном
на рис. 14 А. Стенки органа состоят из покровного эпителия (7)
и лежащего под ним толстого соединительно-тканного слоя (10).
В середине хобота располагается глотка и пищевод, отделенные от
стенок пространством кровеносного синуса (6), образующего от-
четливо выраженную полость хобота. Никаких рудиментов ретракторов
в нем обнаружить не удается. На уровне ложной мантии полость без
резких границ переходит в головной кровеносный синус (5).
Покровный эпителий состоит из опорных и железистых клеток
/рис. 15 (2, 3)/. Поверх него обычно присутствует бесструктурный
слой неясного происхождения (1). Расположенная глубже соедини-
тельная ткань /рис. 16/ содержит многочисленные мускульные волокна,
имеющие по периферии продольную и кольцевую ориентацию, а в глубо-
ких слоях лежащие безпорядочно. Обилие мускульных элементов ука-
зывает на то, что хобот обладает некоторой способностью к актив-
ному движению. *
Выше уже отмечалась большая изменчивость хобота. Она касается
не только его размеров, но и степени развития кровеносного синуса,
мускулатуры и т. д.
На рис. 14 А схематически изображен продольный разрез через
развитый хобот. Он представляет собой массивный вытянутый орган
с обширным кровеносным синусом. Глотка занимает лишь передний
участок хобота, почти вплотную прилегая к его стенкам. Полость
вокруг нее развита слабо. В центре проксимального конца,
хобота прямой трубокой проходит пищевод. Кровеносный синус
вокруг него развит сильнее и далее назад сливается с головным, в
котором лежат ганглии около пищеводного кольца.
На рис. 14 Б представлен продольный разрез через передний
конец тела другого экземпляра, совершенно лишенного хобота. Рото-
вое отверстие (13) у него лежит на очень небольшом возвышении
стенки тела. Глотка (11) расположена на уровне основания мантии
(4) в непосредственном соседстве с околопищеводным нервным коль-
1) Среди Stiliferidae описаны две лишенные раковины Формы:
Gasterosiphon deimatis (Koehler et Уапеу) и Diacolax cucumariae
Mandahl-Barth. Однако сведения O'NEPBOM животном
(Koehler et Vaney, 1903) вызывают сомнения, Т.к. моллюск обла-
дает спирально закрученным внутренностным мешком. По всей вероят-
ности, раковина этого моллюска растворилась при фиксации.
Что касается Diacolax, то его без сомнения следует отнес-
ти к Entoconchidae, поскольку основной аргумент автора
(Mandhal-Barth, 1945 - 46) о разной природе псевдопаллиума у
Eulimidae и Entoconchidae ‘`несостоятелен (см. сноску на стр. 132).
128 DB. "E "TEYSOB
0:025mm
Puc. 15. Asterophila japonica. Puc. 16. Asterophila japonica,
FIG. 15. Наружный покровный эпи- FIG. 16. Участок соединительной
телий. Маллори. ткани хобота. Маллори.
1 - бесструктурный слой; 1 - мускульные волокна;
2 - опорные клетки; 2 - клетки веоединитель-
3 - железистые клетки; ной ткани;
4 - базальная мембрана; 3 - основное вещество.
5
- соединительная ткань.
Asterophila japonica. External Asterophila japonica. Part of con-
surficial epithelium. Stained with nective tissue of snout. Stained
Mallory’s. 1 - structureless layer; with Mallory’s. 1- muscle fiber;
2 - supporting cells; 3 - glandular 2 - cell of connective tissue; 3-
cells; 4 - basal membrane; 5- ground substance.
connective tissue.
yom (15). Эпителий пищевода образует несколько складок, что ука-
зывает на известное сокращение переднего конца тела, однако оно, по-
видимому, невелико и не может объяснить полное исчезновение хобота.
Формы, изображенные на рис. 14, являются крайними в ряду из-
менчивости хобота и встречаются сравнительно не часто. Подавляю-
mee большинство экземпляров Asterophila, как и особи, изученные
Рандаль и Хизом, занимают промежуточное положение.
У самцов хобот всегда отсутствует или представлен очень невы-
сокой ротовой папиллой, к которой название "хобот" применить
очень трудно.
Крайние различия в степени развития хобота столь существенны,
что при отсутствии переходных состояний смогли бы послужить кри-
териями для установления самостоятельных видов. Подобный размах
ASTEROPHILA JAPONICA 129
изменчивости, указывая Ha направление эволюции хобота в сторону
его упрощения, в то же время свидетельствует о TOM, что Формооб-
разовательные процессы у Asterophila к настоящему моменту еще
не закончились.
Редукция хобота происходит у большинства прикрепленных пара-
зитических Melanellidae и Stiliferidae. В ряду Мистопайа
eburnea Deshayes - Parastiliferl - Megadenus (xpome M. arrhynchus)
Stilifer наблюдается постепенное упрощение этого органа.
Полость его зарастает соединительной тканью, а ретракторы исчезают
( Nierstrasz, 1913; Schepman und Nierstrasz, 1913; Rosen,
1910; Иванов, 1952). Однако полное исчезновение хобота наблю-
дается только у Megadenus arrhynchus, хотя здесь остаются еще
рудименты ретракторов (Иванов, 1952), и у высших Entoconchidae
(Bonnevie, 1902; Иванов, 1947).
Сохранению хобота у Stiliferidae способствует выполнение
им Функции прикрепления к хозяину. Возможно, что полная редукция
хобота у эктопаразитов становится возможной только при наличии со-
сательной глотки (М. arrhynchus, Asterophila ).
3. Ложная мантия
Ложная мантия начинается вокруг проксимального конца хобота,
и, простираясь назад, одевает все тело животного. Связь моллюска
с внешней средой осуществляется через отверстие на брюшной стороне
псевдопаллиума, которое представляет собой наружное (вторичное)
‚ половое отверстие: через него происходит копуляция и выходят на-
ружу личинки, развивавшиеся в ложномантийной полости. Характерно,
что при растяжении ложной мантии расстояние между отверстием псев-
допаллиума и половым отверстием остается неизменным.
Как у большинства паразитических моллюсков, ложная мантия
Asterophila представляет складку покровов хобота. В соответствии
с этим гистологически она образована двумя комплексами тканей:
наружным и внутренним, представляющими как бы зеркальное отображе-
ние друг друга /рис. 17/. Каждый комплекс складывается из TIDK-
ровного эпителия и подстилающей его соединительной ткани, содержа-
щей мускульные элементы.
Наружный покровный эпителий (3) во всем подобен эпителию хо-
бота и составляет с ним одно целое. Лежащая под ним соединитель-
ная ткань образована некрупными, рыхло лежащими клетками (7),
между которыми проходят мускульные волокна, которые в своей
совокупности образует два слоя мускулатуры: наружный (5) и вну-
тренний (6). Направление волокон в каждом слое. можно уяснить из
схемы, приведенной на рис. 18. Наружный слой спереди переходит
в слой кольцевых мышц хобота, а внутрений - в слой продольных мышц,
так что мускульные волокна покровов, взятые в целом, располагаются
1) Stilifer sibogae Y St. sp. Schepman et Nierstrasz
выделены Ивановым (1952) в новый род Parastilifer Ivanov.
130 E. H. ГРУЗОВ.
1 - наружный комплекс тка-
ней; 2 - внутренний комп-
лекс тканей; 3 - неружный
покровный эпителий; 4 -
базальная мембрана; 5 -
кольцевые мускульные во-
= = локна; 6 - продольные мус-
SE $ кульные волокна; 7 - клет-
ки соединительной ткани;
8 - кровеносная лакуна;
9 - амебоциты; 10 - основ-
ное вещество соединитель-
ной ткани; 11 - внутренний
покровный эпителий.
ES
Da:
PI
oS
Asterophila japonica. Section
through pseudopallium. Stained
with Mallory’s. 1 - external tis-
sue complex; 2 - internal tissue
complex; 3- external surficial epi-
thelium; 4 - basal membrane; 5 -
0-0 5 = transverse muscle fiber; 6 - longi-
tudinal muscle fiber; 7 - cell of
connectivetissue; 8 - blood lacuna;
Puc. 17. Asterophila japonica. 9 - amebocyte; 10 - ground sub-
FIG. 17. Разрез через ложную мантию. stance of connective tissue; 11-
Маллори. internal surficial epithelium.
по параллелям и меридианам между двумя полюсами, из которых одним
служит ротовое отверстие, а другим - отверстие ложной мантии.
В соответствии с асимметричным положением второго отверстия на
брюшной стороне тела, нарушается также и радиальная симметрия в
расположении мускулатуры ложной мантии, характерная для всех
Entoconchidae. Тем не менее гомология наружного слоя слою коль-
цевых, а внутреннего - слою продольных мышц псевдопаллиума других
моллюсков не вызывает сомнения. У Asterophila продольная ось
ложной мантии оказывается изогнутой на брюшную сторону и не сов-
падает с передне - задней осью тела животного, и морфологически
задний конец этого органа находится не в точке, противоположной
ротовому отверстию, а в участке, занимаемом наружным IIOJIOBBIM
отверстием.
Внутренний комплекс тканей ложной мантии /рис. 17 (2)/
имеет обратное расположение слоев: снаружи, то есть в непосредст-
венном соседстве с внешним комплексом, залегает богатая мускулату-
рой соединительная ткань, глубже находится внутренний покровный
эпителий (11), клетки которого свободными концами обращены внутрь
полости ложной мантии.
Этот эпителий /рис. 19/ значительно ниже наружного и часто
ASTEROPHILA JAPONICA 131
ной мантии.
1 - кольцевые волокна;
2 - продольные волокна;
3 - отверстие ложной
И 1 мантии;
OI
LP
Orientation diagram of muscle fi-
bers in the pseudopallium. 1 -
transverse fibers; 2 - longitudinal
Рис. 18. Схема ориентации мус- fibers; 3- opening of pseudopal-
FIG. 18. кульных волокон в лож- lial cavity.
при сокращении псевдопаллиума становится складчатым. OH образован
невысокими цилиндрическими клетками, несущими довольно длинные
реснички (1). Изредка в эпителии встречаются вытянутые, ли-
шенные ресничек клетки с более густой протоплазмой (2). Их бога-
тые хроматином ядра сильно сдавлены и слегка оттеснены к базальной
мембране. Секреторная Функция этих клеток не исключена.
Мускульные волокна внутреннего комплекса располагаются в два
слоя и имеют то же направление, что и во внешнем комплексе /рис.
17/, однако продольные мышцы (6) лежат здесь снаружи от кольцевых
(5). Оба слоя, а в особенности слой кольцевых мышц, значительно
мощнее соответствующих слоев наружного комплекса.
Между слоями продольных и кольцевых мускульных волокон в сое-
динительной ткани внутреннего комплекса проходят мощные нервы, от-
’ходящие от церебральных ганглиев /рис. 32 - 35 (13)/. Эти нервы,
по три с каждой стороны, прослеживаются на некотором расстоянии
в толще ложной мантии, а затем теряются.
На границе между комплексами имеются лакуны кровеносной си-
стемы. Обилие их во всей ложной мантии свидетельствует о сущест-
венной роли этого органа в процессе дыхания животного. В основа-
нии псевдопаллиума лакуны вступают в связь с головным кровеносным
синусом.
Оба комплекса псевдопаллиума послойно переходят друг в друга
через отверстие ложной мантии, и при этом кольцевые волокна кон-
центрируются вокруг отверстия, образуя его сфинктер. В нормаль-
Азокармин по Гейденгайну.
1 - ресничные клетки;
2 - железистые клетки;
Internal surficial epithelium of
pseudopallium. Stained with
Рис. 19. Внутренний покровный Heidenhain’s azocarmin. 1- cili-
FIG. 19. эпителий ложной мантии. ated cells; 2 - glandular cells.
132
He th SRPY SOB
эпителий;
- мускульные волокна;
- кровеносные лакуны;
основное вещество;
- внутренний покровный
эпителий.
пром
1
mm Section through stretched part of
pseudopallium. Stained with
; Heidenhain’s azocarmin. 1- exter-
Рис. 20. Разрез через растянутый nal surficial epithelium; 2- muscle
FIG. 20. участок ложной мантии. fibers; 3 - blood lacunae; 4-
Азокармин no Гейденгайну. ground substance; 5 - internal sur-
1 - наружный покровный ficial epithelium.
ном состоянии отверстие закрыто, а его края образуют многочислен-
ные морщины. Покровный эпителий этого участка сильно складчатый.
Отверстие способно значительно увеличиваться за счет растяжения
его стенок.
Псевдопаллиум часто сильно растягивается, особенно в своей
спинной части. При этом оба покровных эпителия вытягиваются на-
столько, что внутренний становится чешуйчатым, и клетки его те-
ряют свои реснички /рис. 20/. Все элементы соединительной ткани
также истончается и становятся едва различимыми. Правильность в
расположении мускульных волокон пропадает.
Псевдопаллиум Asterophila бесспорно гомологичен ложной
мантии Stiliferidae и Entoconchidae (1и представляет сильно
разросшуюся кольцевую складку покровов. Иннервация его внутренних
(морфологически задних) частей от церебральных ганглиев свидетель-
ствует о головной природе этого образования.
Морфологические изменения псевлдопаллиума в процессе эволюции
паразитических Melanellidae - Entoconchidae достаточно известны.
( Schiemenz, 1889; Rosen, 1910; Иванов, 1946 и др.). Однако
с функциональной стороны этот вопрос требует дополнительного рас-
смотрения.
Ложная мантия возникает у свободно передвигающихся полупарази-
тических Melanellidae (Koehler et Vaney, 1912; Fretter,
1955) в виде небольшой кольцевидной складки вокруг основания хобо-
та. Назначение подобного образования заключается в том, что оно
изолирует дистальный конец хобота моллюска от внешней среды и
предотвращает проникновение воды в ранку и вымывание пищеваритель-
ных секретов и соков хозяина.
al
Теория Мандаль - Барта (Heding and Mandahl-Barth, 1938),
по которой выводковая камера и сифон Entocolax представляют
дистальный участок гонодукта, покрытый снаружи модифицированной
мантией (и, следовательно, эти органы не гомологичны ложной мантии
Stiliferidae ) была обсуждена и опровергнута Ивановым (1953).
ASTEROPHILA JAPONICA 133
Puc. 21. Мантийный эпителий. Жид-
FIG. 21. кость Флемминга, желез-
ный гематоксилин Гейден-
гайна, тодуидинблау.
1 - базальные ресничные
зерна;
- ресничные клетки;
- включения;
железистые клетки;
- базальная мембрана;
- соединительная ткань;
- слизистые клетки.
NO 01 & WM
1
Pallial epithelium. Fixed with
Flemming’s mixture. Stained with
Heidenhain’s iron hematoxylin,
toluidine blue. 1— basal granule;
2 - ciliated cells; 3- inclusions;
4 - glandular cells; 5 - basal mem-
brane; 6 - connective tissue; 7 -
mucus cells.
У эктопаразитов, обитающих в стенке тела иглокожих, псевдопал-
лиум разрастается и заворачивается назад на раковину ( Megadenus,
Stilifer ). Здесь он служит для фиксации паразита на хозяине и
одновременно создает полость, соединяющую мантийную полость с внеш-
ней средой. Мерцательный эпителий внутренней поверхности ложной
мантии создает ток воды, омывающей жабру и выносящей наружу яйца,
продукты обмена и экскременты животного. Эта новая Функция - осу-
цествленение связи организма с внешней средой - сохраняется за
псевдопаллиумом в процессе дальнейшей эволюции и возможно служит
причиной того, что орган удерживается даже у крайне деградирован-
ных Entoconchidae.
y Asterophila 5 результате обитания в глубоких слоях стенки
тела хозяина, на ложную мантию возлагается задача газообмена, и
при этом утрачивается значение псевдопаллиума как органа, вентили-
рующего мантийную полость. Существенно также превращение полости ложной
мантии в выводковую камеру, - Функция также сохраняющаяся за псев-
допаллиумом на продолжении всей дальнейшей эволюции паразитов, свя-
занных с Melanellidae.
У Entoconchidae к ложной мантии переходит роль экскреторного
органа, a y ЁЕщетохепо$ и Parenteroxenos - также и Функция вса-
сывания питательных веществ. Кроме того, у эндопаразитов ложная
мантия снова используется для прикрепления к кишечнику хозяина.
4. Мантия и мантийный комплекс органов.
Мантия располагается на передней поверхности внутренностного
134
E. H. ГРУЗОВ
мешка Ha левой стороне тела /рис. 7, 8, 9/. Она имеет вид узкой,
нависающей вперед складки. Ограничиваемая ею мантийная полость
невелика, вход в нее, напротив, очень широк.
Мантийную складку и всю переднюю поверхность внутренностного
мешка одевает железистый эпителий. Строение его весьма характерно
Он образован чередующимися ресничными /puc. 21 (2)/u секреторными
(4,7) клетками, первые из которых имеют суженный базаль-
ный конец и расширенную дистальную часть, а вторые - наоборот.
В соответствии с этим ядра клеток располагаются в два отчетливо
выраженных ряда: базальный и дистальный.
`Железистые клетки, в свою очередь, дифференцированы на два
типа. Одни из них (7) окрашиваются бисмаркбрауном в желтый цвет,
a толуидинблау - в фиолетовый, T. €. содержат слизистый секрет,
оформленный в округлые капли.
Клетки другого сорта (4) не содержат слизи, и их секрет собран
в мелкие зернышки или капельки, слегка чернящиеся железным гема-
токсилином. Кроме такого рода включений, протоплазма этих клеток
содержит еще довольно крупные, неправильной Формы глыбки, которые
после осмиевой фиксации и окраски железным гематоксилином приобре-
тают глубокий черный цвет (3).
Описанные клетки чрезвычайно сходны со слизистыми клетками гоно-
дукта.
Мантийный комплекс органов расвнался и частично редуцировался.
Ктенидий, осфрадий, гипобранхиальная железа и ректум исчезли, а по-
ловое отверстие вынесено за пределы мантийной полости на правую
сторону тела. Только почка сохранила примитивные отношения и от-
крывается в глубине мантийной полости.
В связи с тем,что внутренностный мещок утратил спиральную
закрученность, почка, перикардий иматка испытывают смешение Ha
по левой стороне тела, а последний-по правой.
левой стороне тела, а последний - по правой.
Несмотря на изменение топографии мантийного комплекса органов,
основной план строения моллюска не нарушается: почка и перикардий
по-прежнему располагаются слева от ноги, а гонодукт - справа от нее.
Между Tem, Рандаль и Хиз ( Randall et Heath, 1912) отмечают,
что перикардий и почка Asterophila лежат на правой стороне, a ди-
стальные части гонодукта - на левой. Такое же взаимное расположе-
ние органов изображают они на рис. 1 и 2 таблицы 1. Вопрос о топо-
rpadun рассматриваемых органов имеет принципиальное значение, т.к.
оказывает существенное влияние на выводы о Ффилогенетических взаимо-
отношениях нашего вида с другими моллюсками. Поэтому мною было
просмотрено большое число особей Asterophila, и в результате я
пришел к убеждению в ошибочности описания Рандаль и Хиза.
Редукция мантии у паразитических Gastropoda, повидимому,
очень тесно связана с исчезновением раковины. Во всяком случае все
Формы с раковиной имеют нормально развитую мантию, а их мантийный
комплекс варьирует лишь в деталях. Изменения касаются степени
развития жабры, осфрадия и гипобранхиальной железы, причем послед-
ние два органа, а также ректум могут совсем исчезнуть. Так, осфра-
And: отсутствует у Eulima acutissima Swb. (Risbec, 1954), Megadenus
holothuricola Rosen (Rosen, 1910) и несколько недоразвит у M.
arrhynchus (Иванов, 1952). У некоторых экземпляров Рата-
stilifer sibogae отсутствуют прямая кишка и анальное отверстие
ASTEROPHILA JAPONICA 135
(Jonker, 1916). Гипобранхиальная железа недоразвита y
Stilifer celebensis (Иванов, 1952) и отсутствует y Eulima equestris
(Koehler et Vaney, 1912), E. sp. Risbec E. acutissima
(Risbec, 1954) и ap. Однако эти изменения не нарушают об-
щего плана строения всего комплекса органов.
С другой стороны, даже у самых примитивных из Форм, утратив-
ших раковину, мантия всегда рудиментарна, а мантийный комплекс под-
вергается перестройкам, сходным с теми, которые произошли у
Asterophila. У Molpadicola orientalis Grusov мантийная полость
еще сравнительно велика, но в нее открывается лишь почка; органы,
располагавшиеся на потолке полости, исчезли; остальные (матка, рек-
тум) оказались вынесенными за ее пределы (Грузов, 1957). Небольшой
рудимент мантии, прикрывающий только отверстие почки, сохранился
также у Paedophoropus (Ivanov, 937). У всех Entoconchidae
мантия окончательно исчезает.
Из мантийного комплекса, по-видимому, первым исчезает осфра-
дий. Гипобранхиальная железа может дегенерировать очень рано, но
может сохраняться и у глубоуо измененных паразитов. Редукция жабры
происходит, вероятно, одновременно с мантией. Редукция задней киш-
ки и анального отверстия сопряжены в большей степени с изменениями
пищеварительной системы, чем с мантийным комплексом. Дольше всех
удерживает связь с мантийной полостью почка.
Условия для редукции раковины и мантии подготовлены всем
ходом филогенетического развития паразитов. Обитание в толще сте-
нок хозяина и в его внутренних органах делает ненужным сумествование
раковины. Также излишней становится защита органов мантийного ком-
плекса, главным образом, из-за развития ложной мантии. Едва ли не
основной причиной исчезновения мантии можно признать ее топографи-
ческое полпжение: складка, направленная свободным краем вперед,
оказывается невыгодной при погружении паразита в стенку хозяина,
т.к. вход в ограничиваемую ею полость становиться затрудненным.
Рис. 22. Нога. Ложная мантия уда-
FIG. 22. лена, оставшийся лоскут
отогнут.
1 - задняя лопасть ноги;
2 - внутренностный мешок;
3 - ложная мантия;
4 - передняя лопасть ноги.
Foot. Pseudopallium removed, ге-
mainder folded back. 1 - posterior
part of foot; 2 - visceral mass; 3 -
pseudopallium; 4 - anterior part
of foot.
136 E. Н. ГРУЗОВ
5. Нова.
Нога Asterophila низведена до степени небольшого рудимента,
расположенного на внутренностном мешке около основания ложной ман-
тии /рис. 22/. Глубоким поперечным вдавлением нога разделена на
две части и перегнута в этом месте пополам. В результате перегиба
передняя, большая лопасть ноги обращена к вершине внутренностного
мешка /рис. 6/ и полностью (или почти полностью) прикры-
вает небольшую заднюю лопасть. В описании, сделанном Рандаль и
Хизом, задняя лопасть не упомянута.
Если отогнуть переднюю лопасть вперед /рис. 22/, становится
заметной поверхность между обеими лопастями, покрытая многочислен-
ными поперечными складками, между которыми проходят не столь глу-
бокие продольные морщинки. Морщинистый участок имеет более или
менее овальную Форму и вытянут в передне-заднем направлении. Изу-
чение срезов показывает, что он состоит из педальной соединитель-
ной ткани. Задняя лопасть приподнимается над морщинистым участком
в виде небольшого конического бугорка (1).
Гомология частей ноги не вызывает сомнения: передняя доля от-
вечает проподиуму, задняя - метаподиуму, а складчатая поверхность
между ними - подошве других Форм.
Нога у самцов развита несколько лучше, чем у самок. Внешне она
также поделена глубокой перетяжкой на передний и задний отделы,
приблизительно равной величины /рис. 10 (3)/. Морщинистость ноги
незначительна. У молодых Форм в переднем отделе есть небольшой
рудимент педальной железы, полностью исчезающий с возрастом. BTo-
рая педальная железа и крышечка постоянно отсутствуют.
Снаружи нога одета ресничным эпителием /рис. 23/. Он состоит
из высоких цилиндрических клеток и в большей своей части имеет
складчатый характер.
IS Рис. 23. Продольный разрез через
SA FIG. 23. переднюю лопасть ноги.
yy +0 De Азокармин no Гейденгайну.
Sue À y 1 - продольные мускульные
za aS. волокна;
ENDS 2 - соединительная ткань;
oF 3 - покровный эпителий;
Oe 4 - базальная мембрана;
5 - мускульные волокна.
Longitudinal sectionthrough anteri-
or part offoot. Stained with Heiden-
hain’s azocarmin. 1 - longitudinal
muscle fibers; 2 - connective tis-
sue; 3- surficial epithelium; 4 -
O:5mm_ basal membrane; 5- muscle fibers.
ASTEROPHILA JAPONICA 137
O-5mm
Рис. 24. Продольный разрез через эпителий;
FIG. 24. тело самца. Железный ге- 13 - внутренний покров-
матоксилин, лихтгрюн. ный эпителий.
1 - эпителий внутренност-
ного мешка;
- семенник;
- пенис;
- ресничная борозда;
a Longitudinal section through body
4
5 - ложная мантия;
6
if
8
of male. Stained with iron hema-
toxylin, light green. 1 - epithelium
of visceral mass; 2- testis; 3-
penis; 4- ciliated groove; 5-
pseudopallium; 6 - pseudopallium
- ложная мантия самки;
- педальный ганглий;
- рудимент педальной of female; 7 - pedal ganglion; 8 -
железы; vestige of pedal gland; 9- foot;
9 - нога; 10 - печень; 10 - liver; 11 - connective tissue;
11 - соединительная ткань; 12 - external surficial epithelium;
12 - наружный покровный 13 - internal surficial epithelium.
Вся толща ноги заполнена соединительной тканью /рис. 23 (2)/,
в которой проходят мускульные волокна (5), приуроченные главным об-
разсм к периферии органа. В центре ноги мускульные элементы немно-
гочисленны, что свидетельствует о полной редукции колюмеллярного
мускула.
Педальная железа молодых мужских особей имеет Форму небольшого
круглого пузырька, погруженного в соединительную ткань ноги /рис.
24 (8)/. Образующие железу крупные вакуолизированные клетки плотно
прижаты друг к другу и лишены видимого секрета. К переднему краю
железы подходит короткий канал, открывающийся наружу между основа-
нием передней лопасти ноги и ложной мантией. Положение железы сви-
детельствует о ее гомологии с передней (краевой) железой других
моллюсков.
Как самый факт существования ноги у Asterophila, так и силь-
ная ее дегенерация не представляют ничего неожиданного. Редукция
138 Kd Ну MTEYSOB
ноги свойственна паразитическим моллюскам при переходе их к сидя-
чему образу жизни; однако полное ее исчезновение наблюдается у
сильно специализированных Entoconchidae. Процесс редукии иллю-
стрируется следующим морфологическим рядом: Melanella - Mucronalia
- Megadenus - Stilifer, - Parastilifer - Gasterosiphon -
Entoconchidae.
Все исключения из этого правила ( Megadenus arrhynchus,
Stilifer celebensis Kükenthal, Paedophoropus dicoelobius Ivanov
и др. имеют хорошо развитую, хотя и измененную ногу) объясняются
тем, что нога приобретает новые, не локомоторные функции ( Ivanov,
1937; Иванов, 1953; Hirase, 1932).
По степени редукции ноги Asterophila оказывается Ha одной
ступени с Gasterosiphon, хотя характер изменения органа в обоих
случаях различен: у Gasterosiphon нога сохраняется в виде боко-
вых складочек, у Asterophila - передней и задней.
Присутствие у Asterophila — рудимента метаподиума оказывается
важным для понимания его систематического положения и эволюции:
деление ноги на про - и метаподиум из всех паразитических моллюс-
ков наблюдается только у некоторых Melanellidae и низших Stili-
feridae; y высших Stiliferidae и Paedophoropodidae oo от-
сутствует. Между тем, по уровню общей организации Asterophila
бесспорно приближается к последним формам. Подобное несоответствие
указывает на особый путь эволюции А. japonica, но не может пре-
пятствовать сближению ее с группой Stiliferidae - Entoconchidae,
поскольку в эмбриональном развитии Hora представителей этих семейств
обнаруживает ясное деление на переднюю и заднюю доли.
6. Пищеварительная система,
Пищеварительный анпарат /рис. 25/ состоит из глотки, пищевода
и пищаварительной железы, или печени.
Рис. 25. Пищеварительная система.
FIG. 25. Ложная мантия удалена,
стенка тела вскрыта.
1 - яичник; 2 - печень;
3 - яйцевод; 4 - пищевод;
5 - глотка; 6 - дивертику-
лы глотки;
7 - ротовое отверстие;
ложная мантия;
9 - мантия.
00
|
Alimentary system. Pseudopallium
removed, body wall opened. 1-
ovary; 2- liver; 3- oviduct; 4 -
esophagus; 5- pharynx; 6 - pha-
ryngeal diverticulum; 7 - opening
of mouth; 8 - pseudopallium; 9 -
mantle.
ASTEROPHILA JAPONICA 139
IO TES
Глотка представляет собой овальный в продольном сечении или
же цилиндрический орган, полость которого сильно расширена по
сравнению с полостью пищевода /рис. 14/. Язык, радула и
челюсти в ней отсутствуют. Спереди глотка открывается наружу ро-
товым отверстием, а сзади соединяется с пищеводом.
На переднем конце органа глоточный эпителий образует два сле-
пых кармана глотки, лежащих в толще соединительной ткани BO ŸPOH-
тальной плоскости /рис. 25 (6)/. Рандаль и Хиз считают эти обра-
зования рудиментами слюнных желез. Они имеют вид небольших пузырь-
ков, обычно шаровидной формы, но у некоторых индивидуумов сильно
увеличиваются в размерах, и их стенки становягся складчатыми, что
соответствует описанию Рандаль и Хиза. Просмотр большого коли-
чества экземпляров Asterophila показывает, что складчатость сте-
нок этих выпячиваний встречается не часто. С полостью глотки ди-
вертикулы связаны каналами /рис. 12, 13/, часто столь короткими,
что правильнее говорить о непосредственном соеднении глотки с
дивертикулами.
Глоточный эпителий /рис. 26/ состоит из невысоких цилиндри-
ческих или кубических клеток, несущих реснички, под которыми хо-
рошо заметны базальные зерна. Спереди эпителий переходит
в покровный эпителий хобота, а сзади - в эпителий пищевода. Ни-
каких железистых клеток (ни расположенных среди обычных эпители-
альных, ни погруженных под базальную мембрану) в нем обнаружить
1 - клетки соединительной
ткани; 2 - продольные
мышцы; 3 - ядра мус-
кульных клеток;
- основное вещество;
радиальные мускуль-
ные волокна; 6 - коль-
цевые мускульные во-
локна; 7 - базальная
мембрана; 8 - эпителий
глотки; 9 - базаль-
ные ресничные зерна.
or
!
Part of anterior section through
pharynx. Stained with Heidenhain’s
azocarmin. 1 - cell of connective
tissue; 2- longitudinal muscle;
3 - nucleus of muscle cell; 4-
ground mass; 5- radial muscle
fibers; 6 - transverse muscle fi-
Puc. 26. Участок поперечного раз- bers; 7 - basalmembrane; 8 - epi-
FIG. 26. реза через глотку. Aso- thelium of pharynx; 9 - basal gran-
кармин по Гейденгайну. ще.
140
Е. Н. ГРУЗОВ
не удалось. Это обстоятельство кажется особенно удивительным,
т. к. Рандаль и Хиз ( Randall et Heath, 1912) описали погружен-
ные железистые клетки, открывающиеся темно окрашивающимися прото-
ками между клетками эпителия. Однако изображения их авторы не при-
водят, и решить, с какими именно образованиями они имели дело, не-
возможно.
Строение глоточного эпителия несколько меняется в области бо-
ковых карманов глотки. На протяжении каналов, соединяющих их с
полостью глотки, он делается ниже, становясь кубическим и далее -
плоским, и теряет реснички. Базальные зерна ресничек рассмотреть
в нем не удается. Секреторная Функция этого эпителия категоричес-
ки исключается.
Снаружи от глоточного эпителия находится слой соединительной
ткани, богатой мускульными элементами /рис. 26/. Сразу за базаль-
ной мембраной эпителия лежит слой кольцевых мышц (6), а глубокие
слои соединительной ткани пронизаны радиальными волокнами (5).
Кроме упомянутых мускульных волокон, в стенке глотки присутствуют
отдельные, редкие волокна продольного направления (2). Они лежат
снаружи от кольцевых и обособленного слоя не составляют. Спереди
кольцевые и продольные мышцы глотки продолжаются в стенках хобота..
Обилие радиальных мускульных волокон и отсутствие в глоточном
эпителии железистых клеток свидетельствуют о сосательной Функции
органа..
Из рис. 26 видно, какое сильное развитие в стенках глотки полу-
чает основное вещество соединительной ткани (4). Оно окрашивается
по Маллори в синий цвет и слегка подкрашивается бисмаркбрауном.
Его волоконца очень нежные и гораздо более тонкие, чем в соедини-
тельной ткани других органов. В основном веществе разбросаны мно-
гочисленные соединительно-тканные клетки с крупными, бедными хрома-
тином ядрами (1); они гораздо обильнее в периферических частях сте-
нок глотки, чем в центре. Ядра мускульных клеток, напротив, рас-
полагаются ближе к полости органа /рис. 26/.
На срезах через стенку глотки встречаются многочисленные нерв-
ные волокна, а около боковых выпячиваний располагаются два неболь-
ших буккальных ганглия.
Чрезвычайно важным для выяснения систематического положения
Asterophila оказывается вопрос о природе слепых карманов TIOT-
ки. Возможно два решения этого вопроса. Следуя за Рандаль и Хи-
зом, можно считать дивертикулы рудиментами слюнных желез. С дру-
гой стороны, можно признать их новообразованиями, не находящими
себе гомологов у других Gastropoda. Какая из этих возможностей
соответствует истине? Бедность рассматриваемых образований морфо-
логическими признаками не дает возможности высказаться по этому
поводу с полной определенностью.
Дивертикулы, несмотря на сильную редукцию, обнаруживают харак-
терное деление на собственно "железу" и ее проток. У некоторых
индивидуумов Asterophila карманы имеют складчатые стенки и по
внешнему виду напоминают слюнные железы брюхоногих. Положение
этих образований в латеральной плоскости, в передней части глотки,-
соответствует месту впадения протоков слюнных желез. Эти факты,
как будто, говорят в пользу представлений Рандаль и Хиза.
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ASTEROPHILA JAPONICA 141
зерна;
базальная мембрана;
3 - кольцевые мускульные
волокна;
4 - продольные мускульные
волокна.
D
р
Part of anterior section through
esophagus. Stained with Mallory’s.
1 - basal granule; 2 - basal mem-
Рис. 27. Участок поперечного разре- brane; 3 - transverse muscle fi-
FIG. 27. за через пищевод. Маллори. bers; 4- longitudinal muscle fi-
1 - базальные ресничные bers.
С другой стороны, полное погружение дивертикулов в ткани глот-
ки совсем необычно для слюнных желез брюхоногих. Полное отсутствие
секреторной деятельности также представляет аргумент в защиту про-
тивоположной точки зрения.
Весьма существенно, что все моллюски (как паразитические, так
и свободноживущие) группы Melanellidae - Entoconchidae , с ко-
торыми Asterophila обнаруживает много общего во всех чертах сво-
его строения, лишены слюнных желез или их рудиментов. Это застав-
ляет нас рассматривать гипотезу Рандаль и Хиза, по крайней мере,
как спорную.
Б. Пищевод
От заднего конца глотки берет начало пищевод, который тонкой
трубкой с нешироким просветом без каких-либо расширений проходит
во внутренностный мешок и впадает в печень. Стенки его образованы
кубическим ресничным эпителием /рис. 27/. Снаружи пищевод одет
слоем кольцевых (3), а затем продольных (4) мускульных волокон
глотки.
Постоянных, встречающихся у всех особей, изгибов пищевода и,
тем более, петель нет. Однако часто на уровне основания ложной
мантии наблюдается его искривление и отклонение от прямого курса,
что объясняется неравномерным растяжением ложной мантии и связан-
ным с этим смещением ротового отверстия в сторону. Именно такая
особь изображена Рандаль и Хизом ( Randall et Heath, 1912) Ha
Fig. 1 nu их работы. Кроме того, часто эпителий пищевода стано-
вится складчатым, что указывает на некоторое сокращение переднего
конца тела животного.
В. Пищеварительная железа. .
Объемистая пищеварительная железа, печень, у женских особей
занимает всю центральную часть внутренностного мешка /рис. 25/.
У половозрелых особей спинная стенка пищеварительной железы по
всей длине образует чрезвычайно глубокую складку, вдающуюся внутрь
органа (3). В глубине сладки вдоль центральной продольной оси тела
проходит яйцевод. Впячивание стенок делит полостьоргана, на две лопасти,
142
Bu Ш. ATEVSOB
охватывающие яйцевод со всех сторон и соприкасающиеся друг с Apy-
гом на спинной стороне тела. В результате печень приобретает вид
баранки, и создается обманчивое впечатление, что женский гонодукт
прободает пищеварительную железу. У самцов и молодых самок подоб-
ное вдавление отсутствует, и гонодукт проходит рядом с боковой
стенкой органа.
Кроме дорзальной складки, имеется целый ряд менее глубоко
вдающихся в полость печени складок. Отграничиваемые ими дольки
соединяются друг с другом и, в конце концов, открываются в централь-
ный просвет пищеварительной железы /puc. 13/.
Внутрь печени ведет единственное отверстие, лежащее на ее пе-
редней стороне, через которое орган соединяется с пищеводом.
Задняя кишка отсутствует.
Гистологическое строение печени сходно у самцов и у самок
/рис. 28/. Стенка органа состоит из типичного для брюхоногих од-
нослойного эпителия, содержащего клетки двух сортов. Основную
массу составляют крупные цилиндрические клетки (2) с вакуолизи-
ровакной протоплазмой, почти не окрашивающейся никакими красите-
лями. Клетки содержат сферические жировые включения (1), приоб-
ретающие после осмиевых фиксаций черный цвет. От дистальных кон-
цов клеток внутрь полости печени отходят какие-то нити, несколько
напоминающие реснички /рис. 28/. Базальные зерна под ними обна-
Рис. 28. Эпителий печени. Жид- 6 - капли секрета;
FIG. 28. кость Флемминга. Желез- 7 - железистые клетки.
ng er en Epithelium of liver. Fixed with
и Flemming’s mixture. Stained with
1 - включения; Heidenhain’s iron hematoxylin. 1-
2 - пищеварительные клет- inclusions; 2- digestive cell; 3-
ки; 3 - базальная basal membrane; 4 - muscle
MeMOpaHa; fibers; 5- connective tissue; 6 -
4 - мускульные волокна; droplets of secretion; 7 - glandular
5 - соединительная ткань; cells.
ASTEROPHILA JAPONICA 143
ружить не удалось. Возможно, что они представляют собой струйки
секрета, выдавленные из клеток при Фиксации животного. Во всяком
случае, отсутствие базальных зерен, не вполне типичный вид самых
"ресничек", а также отсутствие мерцательных элементов в печени дру-
гих паразитических брюхоногих не позволяют считать эти образования
ресничками. Заметим, кстати, что их окраска и окраска плазмы в
дистальном конце клеток совершенно одинаковы.
Клетки другого сорта (7) отличаются меньшей шириной и более
темной плазмой, в которой видны округлые, темные капли какого-то
секрета. Их плазма сильно окрашивается железным гематоксилином.
Строение эпителия печени одинаково на всем протяжении органа.
Никаких намеков на исчезнувший желудок нет.
По строению пищеварительного аппарата Asterophila o6Hapyxu-
вает много общего с паразитическими Melanellidae - Entoconchidae.
Большинство Melanellidae и Stiliferidae обладают
глоткой в общем сходного с Asterophila строения. Существенно,
что во всех случаях она лишена челюстей, языка, радулы и слюнных
желез. Глоточные выпячивания в области глотки известны лишь у
Megadenus holothuricola (Rosen, 1910) u M. voeltzkowi
(Schepman et Nierstrasz, 1913). У обоих видов непарная железа ле-
жит вентрально около переднего конца глотки и погружена в ее стенки.
Проводить гомологию этих образований с какими бы то ни было орга-
нами других Gastropoda едва ли возможно.
Пищевод А. japonica , выстланный мерцательным эпителием, на-
поминает соответствующий орган Pelseneeria stylifera (Turton)
и Entocolax ludwigi (Rosen, 1910; Voigt, 1888). Y остальных
паразитических моллюсков эпителий пищевода He имеет ресничек.
Пищевод Entocolax rimsky - korsakovi Iwanow снабжен многочислен-
ными мешковидными железами (Иванов, 1953). Пример Megadenus
holothuricola, М. voelizkovi и Entocolax rimsky - korsakovi
показывает возможность появления новообразований в районе перед-
ней кишки.
Редукция желудка, задней кишки и изменения печени у Astero-
phila ue представляют ничего неожиданного. Процесс деградации
желудка и субституции его печенью подробно освещен в литературе
(Graham, 1949; Rosen, 1910; Иванов, 1945 u ap.). Asterophila
занимает промежуточное положение между Stiliferidae и низшими
Entoconchidae, более приближаясь к последним.
7. Кровеносная система и органы дыхания.
Кровеносная система Asterophila претерпела сильное вторич-
ное упрощение, касающееся главным образом сосудистого аппарата.
Сердце находится в обширной, выстланной плоским' перитонеальным
эпителием перикардиальной полости, лежащей под левым краем мантии.
Оно состоит из предсердия и желудочка, расположенных так, что BHem-
ний конец предсердия лежит в заднем наружном углу перикардиальной
полости и сообщается с околопочечным CUHYCOM, а желудок подходит
к внутренней стенке перикардия и находится, следовательно, справа
и немного впереди предсердия /рис. 8, 10/. Клапанов между отдела-
ми сердца нет. Стенки как желудочка, так и предсердия весьма мус-
144
Prc.
L
3
ou»
E. Н.. ГРУЗОВ
0-25 тт
29. Фронтальный разрез через
тело самца.
матоксилин,
Железный ге-
лихтгрюн.
наружный покровный
эпителий;2 - семенник;
эпителий внутренност-
ного мешка;
ложная мантия;
соединительная
пищевод;
дополнительная железа;
церебро-плевральная
ганглиозная масса;
буккальные ганглии;
дивертикулы глотки;
глотка; 12 - ротовое
отверстие; 13 - лож-
ная мантия самки;
субинтестинальный
ткань;
ганглий; 15 - печень;
16 - внутренний покров-
ный эпителий.
Frontal section through body of
male. Stained with iron hematoxy-
lin, light green. 1- external sur-
ficial epithelium; 2- testis; 3-
epithelium of visceral mass; 4-
pseudopallium; 5 - connective tis-
sue; 6 - esophagus; 7 - accessory
gland; 8 - cerebro-pleural gangli-
onic mass; 9- buccal ganglion;
10 - pharyngeal diverticulum; 11 -
pharynx; 12- opening of mouth;
13 - pseudopallium of female; 14 -
subintestinal ganglion; 15 - liver;
16 - internal surficial epithelium.
кулисты и образуют множество продольных складок /рис. 8/.
Сосудистая система Функционально заменена, системой кровенос-
ных синусов и лакун /рис. 12, 13 /.
отходящая от желудочка короткая аорта,
внутрь висцерального мешка и скоро впадающая в обширный головной
синус.
Из сосудов сохранилась только
направляющаяся вперед и
Кровь в нем омывает ганглии центральной нервной системы и
прилежащие органы. Спереди синус связан с полостью хобота /рис.14/.
Сзади он продолжается в то,
CUHYCOM:
что может быть названо висцеральным
систему лакун, простирающихся вдоль по гонодукту, между
ASTEROPHILA JAPONICA 145
внутренними дольками печени и среди яйцевых фолликулов, где лакуны
наиболее обширны /рис. 13 /. У самцов кровеносный синус вокруг ce-
менника также весьма объемист /рис. 12 /.
Венозная кровь собирается в предсердие из широкого синуса на
поверхности гонады и печени, и при этом часть ее проходит через
кровеносные лакуны почки, особенно многочисленные около ее Hapyx-
ной стенки и в трабекулах. Циркуляция крови осуществляется, по-
видимому, не только работой сердца, но и сокращением мускулатуры
всего тела.
Специальных органов дыхания нет. Респирация происходит в
сильно разветвленных лакунах ложной мантии, связанных с головным
кровеносным синусом.
Кровеносная система, нормально развитая у ряда эктопаразити-
ческих Stiliferidae, с углублением паразитизма редуцируется.
Вероятно, существует тесная связь между редукцией кровеносной си-
стемы и жабры; во всяком случае, все Формы, утратившие ктенидий,
обнаруживают значительную редукцию сосудов, замещаемых лакунами
первичной полости тела. Хорошей иллюстрацией этого положения слу-
жит Molpadicola orientalis, органы внутренностного мешка кото-
рой почти не подверглись редукции, и потому отсутствие сосудов y
этой формы может быть связано только с исчезновением жабры (Гру-
зов, 1957). Сосуды отсутствуют также у Paedophoropus (Ivanov,
1837), Gasterosiphon (Koehler et Vaney ,1903)u всех Entoconchi -
dae (Bonnevie , 1902; Schwanwitsch, 1917; Иванов, 1947, 1953).
Последние из перечисленных Форм лишены также и сердца.
8. Выделительная система,
Почка, Asterophila представляет обширный орган /рис. 12, 13/,
граничащий с перикардием, лежащим несколько вентральнее. PeHo-
перикардиальное отверстие и нефридиальная железа отсутствуют.
Передний конец почки находится в области мантийной полости, куда,
она открывается небольшим отверстием. Мочеточник отсутствует.
Расширяющей или суживающей отверстие мускулатуры нет.
Стенки органа образуют многочисленные вдающиеся внутрь склад-
ки (трабекулы), анастомозирующие друг с другом и местами образую-
щие губчатую ткань, заполняющую большую часть внутреннего прос-
вета органа. Трабекулы могут отходить от всех стенок почки, но
наружная стенка всегда несет большее их число, и сами складки здесь
крупнее; кроме Toro, трабекулы на наружной стенке появляются в OH-
тогенезе, по-видимому, раньше, чем на внутренней. Количество Tpa-
бекул у самцов меньше, чем у самок.
Однослойный почечный эпителий /рис. Зо/ образован невысокими
цилиндрическими, кубическими или же неправильной Формы многоуголь-
ными клетками, лишенными ресничек. В каждой клетке имеется нес-
колько крупных и большое число мелких вакуолей (2), содержащих раз-
личного размера включения (3), имеющие естественный буровато-серый
цвет и окрашивающиеся по Маллори в синий цвет, а также чернящиеся
железным гематоксилином. Включения, бесспорно, представляют собой
продукты выделения животного.
Таким образом, почка А. japonica мало изменена по сравнению
146 | Е. H. ГРУЗОВ
со свободноживущими Gastropoda. То же можно сказать относи-
тельно этого органа у других паразитических моллюсков Melanell -
idae, Stiliferidael и Paedophoropodidae. Характерно, что
почечные трабекулы здесь располагаюся только на наружной стенке
ODrFAHS MY Entoconchidae почки нет.
Рис. 30. Эпителий почки. Железный
FIG. 30. гематоксилин Гейденгайна.
1 - базальная мембрана;
2 - вакуоли;
3 - конкреции.
Epithelium of kidney. Stained with
Heidenhain’s iron hematoxylin. 1 -
basal membrane; 2 - vacuoles; 3 -
concretions.
9. Нервная система.
А. А. Центральная нервная система.
Центральная нервная система Asterophila имеет следующий
план строения /рис. 31/. Церебральные и плевральные ганглии сли-
ваются друг с другом, образуя общую ганглиозную массу (5, 15), ле-
жащую над кишкой. Вентрально к ним примыкают два педальных ганг-
лия (9), лежащие рядом с основанием ноги. Имеется пара статоциетов
(8), занимающих нормальное положение. В области глотки находятся
два буккальных ганглия (1), прилегающих к боковым дивертикулам киш-
ки и соединяющихся друг с другом комиссурами (2), проходящими над
и под глоткой. По-видимому, имеется соединение буккаьных ганглиев
с церебральными при помощи церебро-буккальных коннективов (3).
Висцеральное нервное кольцо разомкнуто. Одна его половина состоит
из висцерального (4) и субинтестинального (6) ганглиев, связанных
с левой половиной церебро-плевральной ганглиозной массы коннекти-
вом (7), проходящим под кишкой. Другая половина висцерального
кольца содержит единственный супраинтестинальный ганглий (12);
коннектив, соединяющий его с левой половиной церебро-плевральной
массы (14), огибает кишку сверху. Таким образом, наблюдается пе-
рекрест нервных стволов, направляющихся во внутренностный мешок,
т.е. хиастоневрия. От описанного плана строения имеются много-
численные отступления, связанные с изменчивостью топографического
положения отдельных органов, и главным образом, большей или меньшей
изогнутостью пищевода.
1) у Gasterosiphon deimatis почка отсутствует ( Koehler
et Vaney, 1903).
ASTEROPHILA JAPONICA 147
ный коннектив; 8 - cTa-
тоцист; Y - педальные
ганглии; 10 - педальная
комиссура; 11 - нерв ста-
тоциста; 12 - супраинтес-
тинальный ганглий;
13 - нервы ложной мантии;
14 - плевро-супраинтести-
нальный коннектив;
15 - левая половина цереб-
ро-плевральной ганг-
лиозной массы.
lig
Diagram of central nervous system.
Posterior view. 1- buccal gang-
lion; 2 - buccal commissures; 3 -
cerebro-buccal connectives; 4 -
visceral ganglion; 5 - right por-
Puc. 31. Схема строения централь-
FIG. 31. ной нервной системы.
Вид сзади.
Е $ ce + : tion of cerebro-pleural ganglionic
? mass; 6 - subintestinal ganglion;
3 - церебро-буккальные 7- pleuro-subintestinal connective;
коннективы; à £ 8 - statocysts; 9- pedal ganglia;
4 - висцеральный ганглий; 10 - pedal commissure; 11 - nerve
5 - правая половина цереб- of statocyst; 12- supraintestinal
ро-плевральной гангли- ganglion; 13- pseudopallial nerves;
озной массы; 6 - субин- 14 - pleuro-spuraintestinal connec-
тестинальный ганглий; tive; 15 - left portion of cerebro-
7 - плевро-субинтестиналь- pleural ganglionic mass.
У особи, изображенной на puc. 32, плевро-супраинтестинальный
коннектив плотно прижимается к левой половине церебро-плевральной
массы и в одном месте сливается с ней (16), так что на срезах ви-
ден переход волокон из нервного тяжа в ганглий.
В другом случае /рис. 33 Б/ этот коннектив полностью сли-
вается с церебро-плевральной массой и выступает лишь как валик на
ее поверхности.
Часто наблюдается большая концентрация центральной нервной
системы, чем это описано выше. У экземпляра, изображенного на
рис. 34, субинтестинальный (6) и висцеральный (4) ганглии слиты
вместе и отделяются только легкой перетяжкой; кроме того, субин-
тестинальный ганглий частично сливается с правой половиной церебро-
плевральной массы. Таким образом, у данного экземпляра оказывают-
ся слитыми в общую массу шесть ганглиев: два церебральных, два
плевральных, один париетальный и висцеральный.
Обращает на себя внимание сильное развитие части нервной си-
стемы, расположенной в хоботе (16) и образующей плексус симпати-
ческой нервной системы вокруг глотки.
Наконец, в одном случае /рис. 35/ субинтестинальный ганглий
(6) соединяется с правым плевральным (5), но висцеральный (4) да-
леко отстоит от него. Коннектив (7), соединяющий его с париеталь-
148
By H. “EPYSO0OB
Центральная нервная си-
crema. А - вид спереди;
Б - вид сзади. Пласти-
ческая реконструкция.
16 - место соединения
плевро-супраинтестиналь-
ного коннектива с левой
половиной церебро-плев-
ральной массы. Остальные
обозначения как Ha puc.31.
Central nervous system. А, an-
terior view; В, posterior view.
Plastic reconstruction. 16 - point
of fusion of pleuro-supraintestinal
connective with left portion of cere-
bropleural mass. Other numbers
as in Fig. 31.
Центральная нервная си-
стема. А - вид спереди;
Б - вид сзади. Пласти-
ческая реконструкция.
Обазначения как на рис.31.
Central nervous system. А, ап-
terior view; B, posterior view.
Plastic reconstruction. Numbers
as in Fig. 31.
ASTEROPHILA JAPONICA 149
Puc. 34. Центральная нервная систе-
FIG. 34. ma. А - вид спереди; B -
вид сзади. Пластическая
ив Central nervous system. А, an-
16 - нервный плексус глот- terior view; В, posterior view.
ки; 17 - педальный нерв; Plastic reconstruction. 16 -
18 - висцеральный нерв; nerves of pharyngeal plexus; 17 -
19 - церебро-плевро-пе- pedal nerve; 18 - visceral nerve;
дальный коннектив. Осталь- 19- cerebro-pleuro-pedal соппес-
ные обозначения как Ha tive. Other numbers as in Fig.
Brei... 31; 31.
ным ганглием, проходит неподалеку от второго плевропариетального
коннектива (14), и между ними устанавливается связь при помощи
короткого нервного тяжа (16).
Отмеченная пластичность строения центральной нервной системы
иллюстрирует ход и направление ее эволюции в сторону увеличения
концентрации ганглиев. У мужских особей концентрация несколько
меньшая /рис. 29, 36/.
Органы чувств представлены парой статоцистов, лежащих рядом
с педальными ганглиями /рис. 34, Б (8)/. Глаза и щупальцы от-
сутствуют.
Б. Периферическая нервная система.
Наиболее мощные нервы отходят от латеральных частей церебро-
плевральной массы, по три с каждой стороны. Они направляются в
ложную мантию /рис. 31-35/, проходят во внутреннем комплексе тка-
150
Ш. «Не. TPYSOB
1
0-25mm A 0-25mm B
—
Рис. 35. Центральная нервная си-
FIG. 35. стема. А - вид спереди;
Б - вид сзади. Пласти-
ческая реконструкция.
16 - место ‘соединения
субинтестинального ган-
глия с плевро-супраинтес-
тинальным коннективом;
17 - педальный нерв;
18 - нерв субинтестиналь-
ного ганглия. Остальные
обозначения как на рис.31.
Central nervous system. А, an-
terior view; В, posterior view.
Plastic reconstruction. 16 - point
of fusion of subintestinal ganglion
with pleuro-supraintestinal con-
nective; 17 - pedal nerve; 18 -
nerves of subintestinal ganglion.
Other numbers as in Fig. 31.
ней этого органа и легко прослеживаются на значительном протяжении.
Кроме того, от церебро-плевральной ганглиозной массы отходят два
нерва к статоцистам /рис. 34/.
Педальные ганглии /рис. 34/ посылают по два коротких нерва в
ногу (17). У самцов от правого педального ганглия отходит мощный
нерв в основание совокупительного органа.
Пара тонких нервов отходит от супраинтестинального ганглия и
очень скоро теряется в соединительной ткани внутренностного мешка,
в области мантии, перикардия и почки /рис. 33/.
Проследить область иннервации субинтестинального ганглия не
удалось, хотя на некоторых препаратах заметны несколько отходящих
от него тонких нервов /рис. 34/. Около висцерального ганглия на-
блюдался единственный нерв /puc. 33/, проходящий вдоль гонодукта
ASTEROPHILA JAPONICA 151
и вскоре исчезающий.
Нервы, иннервирующие глотку, были описаны выше.
Большинство Melanellidae и Stiliferidae обладают высоко-
развитой центральной нервной системой обычного для Taenioglossa
типа. Она состоит из парных церебральных, плевральных и педальных
ганглиев, соединяющихся друг с другом, а также двух париетальных
и, по-видимому, всегда единственного висцерального гангпия. MHo-
гие представители этой группы ( Melanella polita (Linnaeus), Balcis
devians (Monterosato);, B.alba (Da Costa) Megadenus arrhynchus,
Stilifer celebensis и Gasterosiphon) имеют, кроме того, парные
буккальные ганглии, расположенные в хоботе по соседству с глоткой
и соединяющиеся с церебральными длинными коннективами.
Уже у примитивных форм проявляется тенденция к концентрации
церебральных, плевральных и педальных ганглиев, выражающаяся в их
сильном сближении и укорочении соответствующих коннективов и ко-
миссур, однако ганглии при этом остаются еще вполне раздельными.
Таково строение нервной системы Melanella equestris (Koehler et
Vaney, 1912), Megadenus cysticola Koehler et Vaney
и М. arrhynchus ( Koehler et Vaney, 1912; Иванов, 1952), всех
Pelseneeria (Rosen, 1910), ряда видов Stilifer (Risbec,
1954; Иванов, 1952) и др. Так как подобная степень концентрации
известна еще и у многих свободноживущих Taenioglossa, то весь-
ма вероятно, что она явилась исходным состоянием для всех более
специализированных паразитов, для которых характерно слияние от-
дельных ганглиев друг с другом. При этом оказывается, что плев-
ральные ганглии имеют тенденцию сливаться с церебральными, а це-
ребральные друг с другом. Педальные ганглии обычно остаются само-
стоятельными, но тесно прижимаются к церебральны`. и плевральным,
‚’ а соответствующие коннективы значительно укорачиваются (Иванов,
1952).
Изменения висцерального нервного кольца у Stiliferidae
выражаются в исчезновении осфрадиального ганглия и редукции ряда
ганглиев. Нервное кольцо часто оказывается разомкнутым.
По уровню концентрации нервной системы Asterophila обнару-
живает много общего с Paedophoropus dicoelobius и с некоторы-
ми представителями Stiliferidae .
Редукция центральной нервной системы у Entoconchidae
зашла значительно дальше, и только y Entocolax schwanwitschi
сохраняется рудиментарный церебральный ганглий (Schwanwitsch,
1917). Женские и гермафродитные особи остальных Entoconchidae
полностью лишены нервной системы. В то же время у самцов некото-
рых Entoconchidae, например Entocolax trochodotae, нервная
система развита несколько лучше (Heding, 1934), что стоит в свя-
зи с неотеническим характером этих организмов.
10. Половая система
А. Мужская половая система
Семенник представляет собой обширный мешковидный орган, зани-
мающий большую часть внутренностного мешка, не исключая и вершины
152
E "Ho "EPYSOD
0-25mm 7
Puc. 36. Фронтальный разрез через чень; 17 - эпителий
FIG. 36. тело самца. Железный ге- внутренностного мешка.
матоксилин, лихтгрюн.
1 - семенник; 2 - висце-
ральный ганглий; 3 - на-
ружный покровный эпителий;
4 - соединительная ткань;
5 - внутренний покровный
эпителий; 6 - дополнитель-
ная железа половой системы;
7 - мантийная полость;
8 - ложная мантия;
9 - мантия; 10 - ресничная
борозда пениса; 11 - ди-
Frontal section through body of
male. Stained with iron hematoxy-
lin, light green. 1- testis; 2-
visceral ganglion, 3- external
surficial epithelium; 4- connec-
tive tissue; 5 - internal surficial
epithelium; 6- accessory gland of
reproductive system; 7 - mantle
cavity; 8- pseudopallium; 9 -
mantle; 10- ciliated groove of
вертикулы глотки; 12 - ro- penis; 11 - pharyngeal diverti-
ловной кровеносный синус; culum; 12 - cephalic blood sinus;
13 - педальный ганглий; 13 - pedal ganglion; 14 - pseudo-
14 - ложная мантия самки; pallium of female; 15 - suprain-
15 - супраинтестиналь- testinal ganglion; 16 - Пуег; 17-
ный ганглий; 16 - ne- epithelium of visceral mass.
/рис. 36/. Спереди он граничит с пищеварительной железой, пери-
кардием, почкой и гонодуктом; вся остальная поверхность органа при-
легает к покровам внутренностного мешка, местами отделяясь от них
кровеносными синусами. Снаружи семенник покрыт тонкой соединитель-
но-тканной мембраной.
На срезах через семенник видны картины интенсивного спермато-
генеза. Зародышевые клетки занимают пристеночное положение, а бли-
же к центру органа располагаются сперматоциты на разных стадиях
созревания и зрелые сперматозоиды. У молодых неполовозрелых осо-
бей семенник целиком заполнен половыми клетками и лишен внутреннего
ASTEROPHILA JAPONICA
Рис. 37. Разрез через выводные пути
FIG. 37. мужской половой системы.
Кислый гемалаун Мейера,
бисмаркбраун.
1 - сперматозоиды;
Sr A Section through vas deferens.
3 - эпителий семепровода; Stained with Mayer’s acid haema-
4 - железистые клетки; lum, Bismarck brown. 1- sper-
9 - опорные клетки; matozoa; 2-testis; 3- epithe-
6 - эпителий внутренност- lium of vas deferens; 4 - glandu-
ного мешка; lar cells; 5- supporting cells;
7 - дополнительная железа; 6 - epithelium of visceral mass;
8 - соединительная ткань; 7 - accessory gland; 8 - connec-
9 - семепровод. tive tissue; 9 - vas deferens.
просвета. У старых самцов слой сперматоцитов и сперматогониев
очень TOHOK, и орган имеет обширную внутреннюю полость, в которой
группами и поодиночке разбросаны сперматозоиды.
Часть стенок семенника‘в районе отверстия семепровода образо-
вана кубическим, лишенным ресничек эпителем, переходящим в эпите-
лий гонодукта /puc. 37/.
Семенник соединяется с очень коротким семепроводом, залегаю-
щим под покровами внутренностного мешка на правой стороне тела,
/рис. 37 (9)/. Семепровод представляет собой прямой узкий канал,
который, по всей вероятности, может несколько растягиваться массой
спермы. Его стенки образованы кубическим или цилиндрическим без-
ресничным эпителием (3), клетки которого не содержат никакого сек-
рета. Их округлые ядра занимают центральное положение. Снаружи
базальной мембраны, подстилающей эпителий семепровода, без опреде-
ленной ориентации проходят редкие мышечные волокна.
153
154 Е. Н. ГРУЗОВ
Дистальный участок мужского гонодукта резко выделяется своим
строением, образуя хорошо ограниченную дополнительную железу поло-
вой системы. Спереди она открывается узким щелевидным половым от-
верстием, расположенным на передней поверхности внутренностного
мешка, немного впереди свободного края мантийной складки /рис. 9
Е
Толстые стенки железы образованы высоким эпителием из непра-
вильно чередующихся железистых и опорных клеток /рис. 37/. Желе-
зистые клетки (4) имеют крупные размеры, широкое основание и су-
женный дистальный конец, через который их секрет поступает в по-
лость железы. Протоплазма сильно вакуолизирована и интенсивно ок-
рашивается бисмаркбрауном, так как содержит большое количество
слизистого секрета. Некоторое количество выделившейся слизи всег-
да присутствует и в полости органа.
Опорные клетки (5) значительно уже железистых и равной с ними
высоты. Обычно они располагаются между железистыми клетками, и
тогда их дистальные концы расширяются, а клетки в целом приобре-
тают вид урночек с тонкими стебельками. Ядра находятся в расши-
ренных частях клеток. В тех случаях, когда опорные клетки собраны
группами, они имеют более или менее правильную цилиндрическую форму,
а ядра занимают центральное положение.
Снаружи железа одета тонким слоем мускульных волокон.
Относительно Функции железы можно строить лишь предположения.
Возможно, что выделяемая ею слизь служит той средой, в которой жи-
вут сперматозоиды.
На передней стороне тела справа от ноги помещается penis
животного /рис. 10/. Он представляет собой более или менее цилин-
дрический, пальцеобразный вырост, превосходящий по своей длине вы-
соту внутренностного мешка. Диаметр его постепенно уменьшается
от основания к вершине, а самый конец мягко закруглен. Вдоль
дорзальной стороны органа проходит глубокий желобок, по которому
стекает сперма. Penis способен к значительным мышечным сокрацще-
ниям и может сильно вытягиваться при копуляции. В спокойном со-
стоянии он лежит в ложномантийной полости, прилегая к внутренност-
ному мешку. Многочисленные морщины на его поверхности и значитель-
ная толщина органа при сравнительно небольшой длине указывают на
его сильное сокращение. При копуляции совокупительный орган вытя-
гивается и высовывается через отверстие в ложной мантии; конец его
вводится в наружное половое отверстие самки и, вероятно, проникает
также и в отверстие матки, так как сперма в ложномантийной полости
самок никогда не наблюдалась.
Гистологическое строение органа видно из рис. 24. Складчатый
покровный эпителий образован цилиндрическими, лишенными секрета
клетками с хорошо развитыми ресничками. Около дистального края
клеток присутствует полоска базальных ресничных зерен. Овальные,
небогатые хроматином ядра располагаются в центре клеток. В районе
ресничной борозды (4), проходящей вдоль совокупительного органа,
реснички мерцательных клеток становятся более густыми и длинными.
Специальные железистые клетки нигде не были обнаружены.
Снизу эпителий подстилается базальной мембраной, под которой
залегает соединительная ткань и мускулатура органа. Мускульные
волокна проходят только в продольном направлении и образуют ясно
Puc. 38. Женская половая система.
ЕТа. 38. Вид
ИЕ
O O1 > WwW
|
ASTEROPHILA JAPONICA 155
спереди.
женское половое от-
верстие; 2 - матка;
семеприемник;
белковая железа;
яйцевод;
яичник.
выраженный мускульный слой.
Соединительная ткань представлена,
мало отличающимися от клеток педальной
Female reproductive system. An-
terior view. 1- female genital
opening; 2- pallial oviduct; 3 -
seminal receptacle; 4- albumen
gland; 5- oviduct; 6 - ovary.
неправильной Формы клетками,
соединительной ткани.
Обращает на себя внимание сильное развитие в совокупительном opra-
не кровеносных лакун,
веносным синусом.
эрекцию органа,
ного эпителия.
В толще соединительной ткани проходят нервные волокна, OTXO-
дящие от правого педального ганглия.
соединяющихся, в конце концов, с головным кро-
Наполнение лакун кровью может вызвать сильную
о чем свидетельствует также складчатость покров-
Таким образом, педальное
происхождение пениса не вызывает сомнений.
Б. Женская половая система
Женский половой аппарат /рис. 38/ состоит из яичника (6) и
яйцевода (5), дистальный конец которого подразделяется на три раз-
личных участка: дополнительную, белковую железу (4), семеприемник
(3) и железистую матку (2).
Форма, размеры и положение яичника, естественно, сильно ме-
HAWTCA с возрастом животного.
У самых молодых исследованных эк-
земпляров, далеко не достигших еще половой зрелости, он представ-
ляет небольшую трубку,
спинной стороны внутренностного мешка,
залегающую непосредственно под покровами
правее медиальной линии.
У более сформированных, но не перешедших еще к половой активности
156
fs) Ho ЕРУЗОВ
животных, яичник ветвится так, что боковые отростки отходят в обе
стороны от основного ствола, хорошо заметного, благодаря большим
размерам /рис. 39/. Орган достигает вершины внутренностного меш-
ка и при дальнейшем росте заворачивается на брюшную сторону. Эта
стадия позволяет ясно судить о характере расчленения органа. Ee
самой замечательной особенностью следует признать отхождение боко-
вых ветвей яичника в обе стороны от центрального ствола - черта,
свидетельствующая о глубокой перестройке организма, утратившего
всякие следы спиральной закрученности органов внутренностного меш-
ка даже на ранних стадиях онтогенеза..
о У животных, находящихся в разгаре репродуктивной деятельности,
яичник достигает больших размеров, заполняя вся вершину висцераль-
ного мешка и оттесняя печень вперед. Увеличение его размеров про-
исходит за счет многократного ветвления как главного ствола, так
и боковых ветвей, что приводит к образованию многочисленных долек
органа и к исчезновению разницы в размерах между основным и побоч-
ными его стволами. Рисунок 38 передает Форму яичника на такой
стадии развития. Характерно, что отдельные дольки нигде не ана-
стомозируют, хотя на наружной поверхности яичника они оказываются
тесно прижатыми друг к другу. Сквозь эпителий яичника просвечи-
вают яйца и крупные овоциты, наполненные желтком. Картины овоге-
неза очень напоминают соответствующие стадии овогенеза у Enterox -
enos, описанные Бонневи ( Bonnevie, 1906).
OT переднего конца яичника, из того места, где все трубки
этого органа соединяются воедино, отходят яйцевод. На всем своем
протяжении он проходит в глубокой дорзальной складке печени, так
что при поверхностном изучении создается впечатление того, что он
прободает пищеварительную железу. Иногда яйцевод образует несколь-
ко искривлений, но чаще представляет прямую, сравнительно короткую
трубку с узким просветом. Стенки его лишены внутренних складок,
но тем не менее могут несколько растягиваться во время прохождения
яиц. Около передней поверхности тела он резко вздувается, образуя
добавочную железу, лежащую на спинной стороне /рис. 38/. Железа
имеет яйцевидную форму, и ее расширенная часть сообщается с маткой
и семеприемником. Яйцевод подходит к задней (внутренней) поверх-
ности железы и открывается в нее небольшим отверстием, лежащим
ближе к вентральной стороне органа. Левая часть железы имеет вид
слепо замкнутого мешка.
y
Рис. 39. Яичник и выводные пути
FIG. 39. неполовозрелой самки.
1 - яичник;
2 - яйцевод;
3 - дистальная часть
гонодукта..
Ovary and oviduct of immature fe-
male. 1- ovary; 2- oviduct;
3 - distal part of gonoduct.
ASTEROPHILA JAPONICA 157
Рис. 40. Эпителий дополнительной
FIG. 40. (белковой) железы женской
половой системы. Азокар-
мин по Гейденгайну.
1. - базалвные ресничные
зерна;
2 - ресничные клетки;
3 - железистые клетки;
4 - базальная мембрана.
Epithelium of accessory (albumen)
gland of female genital system.
Stained with Heidenhain’s azocar-
min. 1- basal ciliated granule;
0-025 2 - ciliated cells; 3 - glandular
mm cells; 4 - basal membrane.
Sas
S
Рис. 41. Эпителий семеприемника.
FIG. 41. Азокармин по Гейденгайну. Epithelium of seminal receptacle.
1 - ресничные клетки; Stained with Heidenhain’s azocar-
2 - сперматозоиды; min. 1- ciliated cells; 2 - sper-
3 - базальная мембрана. matozoa; 3 - basal membrane.
158 | Е. H. ГРУЗОВ
Рис. 42. Эпителий матки. Азокар-
FIG. 42. мин по Гейденгайну.
1 - базальные ресничные
зерна;
ресничные клетки;
- железистые клетки;
базальная мембрана;
мускульные волокна.
oF wm
1
Epithelium of pallial oviduct.
Stained with Heidenhain’s azocar-
O-O5mm min. 1- basal ciliated granule;
2 - ciliated cells; 3 - glandular
cells; 4- basal membrane; 5-
muscle fibers.
Tuctonoruueckn яйцевод и железа имеют сходное строение /рис. 40/.
Их эпителий образован чередующимися мерцательными (2) и железисты-
ми (3) клетками, окрашивающимися по Маллори в голубой цвет и, по-
видимому, секретирующими слизистые вещества.
Семеприемник представляет собой выпячивание спинной стенки
гонодукта на границе между дополнительной железой и маткой /рис.
38/. Стенки его имеют многочисленные внутренние складки /рис. 41/,
выстланные мерцательным эпителием. В полости органа постоянно
находится сперма.
Матка расположена на правой стороне передней поверхности
внутренностногомешка, и ее дистальный конец доходит почти до ноги, а
левый край находится на линии соединения внутренностного мешка. с
ложной мантией. Расширенным проксимальным концом она соединяется
с дополнительной железой и семеприемником, а к дистальному концу
постепенно сужается, заостряясь на вершине. В поперечном сечении
орган имеет форму сильно вытянутого эллипса, так как наружная и
внутренняя стенки близко прилегают друг к другу. Длинным и узким
щелевидным отверстием матка открывается в полость ложной мантии
около основания псевдопаллиума. Рандаль и Хиз (Randall et Heath,
1912) правильно описали положение полового отверстия на правой
стороне тела, но на рисунках (Fig. 1-2) изобразили его лежащим
слева.
Толстые стенки органа образованы высоким цилиндрическим эпи-
телием, составленным правильно чередующимися железистыми (слизи-
стыми) и мерцательными клетками /рис. 42/. Неодинаковая высота
клеток в разных участках органа вызывает появление морщин и скла-
док, общее число которых обычно невелико.
Протоплазма железистых клеток наполнена сферическими каплями
или зернами секрета, приобретающего после окраски по Маллори ин-
тенсивно синий цвет. Эти же включения метахроматически окрашивают-
ся толуидинблау в фиолетовый цвет, что указывает на слизистую при-
ASTEROPHILA JAPONICA 159
роду секрета. Ha дистальном конце клетки сужаются и открываются
наружу узкими протоками, проходящими между мерцательными клетками.
Клеточные границы всегда хорошо различимы.
Не все железистые клетки наполнены секретом, многие из них
оказываются порожними. В таком случае в протоплазме присутствует
большое число вакуолей, содержащих лишь отдельные капли секрета,
и они окрашиваются по Маллори в голубой цвет, теряя способность
краситься бисмаркбрауном и толуидинблау.
Матка длинной щелью открывается наружу на правую сторону вис-
церального мешка справа от ноги. Откладываемые яйца склеиваются
в кокон, насчитывающий несколько сотен яиц. Кокон помещается в
псевдопаллиальной полости. и
По строению половой системы Asterophila обнаруживает много
общего с раздельнополыми представителями Stiliferidae и Ento-
conchidae, особенно с некоторыми видами Megadenus, обладающими
дополнительными придатками половой системы.
Выработавшиеся у Asterophila приспособления, обеспечивающие
оплодотворение яиц, т. е. обитание самца на поверхности самки, боль-
mag длина совокупительного органа и др., также находят себе анало-
гию в этой группе паразитических моллюсков. У раздельнополых па-
разитов, обитающих неподвижно в коже хозяина, самцы прикрепляются
всегда рядом с самками, при этом они обычно ок%зываются меньших
размеров ( Возеп, 1910; Иванов, 1941). У многих Entoconchidae
крошечные мужские особи обитают внутри ложномантийной полости са-
мок ( Schwanwitsch, 1917; Иванов, 1953).
Вместе с уменьшением размеров тела самцов происходит процесс
их морфологического упрощения, протекающий параллельно процессу
деградации женских особей. Скорости этих процессов у представите-
лей разных полов, как правило, не совпадают. Самцы крайне спе-
циализированных эндопаразитов ( Entocolax schwanwitschi, Ento-
concha) упрощены сильнее самок. Тело мужских особей Ento-
concha, первоначально ошибочно описанных Мюллером под названием
"семенные капсулы", состоит только из покровов и семенника, все
остальные органы, даже семепровод, исчезли ( Müller , 1852). В To
же время самцы менее специализированных паразитов (Asterophila,
Entocolax trochodotae и др.) во многих отношениях примитивнее
самок. Это выражается или в присутствии у них некоторых органов,
исчезнувших у женских особей того же вида, или же, наоборот, в от-
сутствии или меньшей выраженности признаков, развитых у самок зна-
чительно сильнее.
Существенно, что органы первой категории, например рудимент
ноги Entocolax, отсутствующий у самок, или нервная система
Asterophila, менее концентрированная y самцов, как правило, ис-
чезают в процессе эволюции, а органы второй категории, недоразви-
тые у самцов (ложная мантия, слюнные железы Capulidae и др.),
представляют образования, с углублением паразитизма развивающиеся
прогрессивно. В данном случае характер отличий между особями раз-
ных полов ясно свидетельствует о том, что большинство органов у
мужских особей остановилось на более ранней стадии онтогенетичес-
кого развития, чем у женских. Подобная неотеничность самцов, по-
видимому, характерна для некоторых Stiliferidae, Paedophoropod-
idae u A. japonica.
160
E Ha, DPY30B
Что касается Entoconchidae, To у них для объяснения различий
в уровне организации разных полов недостаточно одного явления нео-
тении. Метаморфоз E. schwanwitschi показывает, что здесь сов-
падают только самые начальные этапы постларвального развития сам-
цов и самок. Дальнейшее развитие самцов сводится к дегенерации
большинства личиночных органов и развитию одной лишь половой сис-
темы, тогда как у самок происходит прогрессивное развитие и ряда
соматических органов: ложной мантии, кишечника и др. Процесс де-
генерации личиночных органов самцов у остальных раздельнополых
Entoconchidae, по-видимому, заходит еще дальше (Шванвич, 1946).
Способ развития полового диморфизма дает некоторые указания
и на возможные причины этого процесса. Выпадение конечных стадий
метаморфоза у примитивных Форм и крайняя простота метаморфоза у
форм редуцированных одинаково ведут к ускорению процесса развития.
Известно, что метаморФоз личинки во взрослого самца начинается
только с момента проникновения ее в самку, которая к этому времени
проделала уже большую часть своего постларвального развития
(Schwanwitsch, 1917). Ускоренное развитие самца, на наш взгляд,
позволяет особям разного пола достигнуть половой зрелости в одно
и то же время и этим повышает плодовитость животного.
в
1У. Организация личинки.
Как уже отмечалось выше, склеенные в кокон яйца
развиваются в ложномантийной полости женских особей до стадии ве-
лигера.
К моменту полного сформирования личинок кокон разрушается и
7
Рис. 43. Внешний вид велигера.
FIG. 43. A - вид с брюшной стороны;
Б - вид слева.
1 - парус; 2 - щупальца; Ventralviews of veliger. A, view
3 - ротовое отверстие; of ventral surface; В, view from
= SS left. 1- velar lobes; 2 - tenta-
HOM железы; cles; 3- opening of mouth; 4-
5 - задняя лопать ноги; opening of gland of sole; 5 - pos-
6 - крышечка; terior part of foot; 6-operculum;
7 - раковина; 7 - shell; 8 - anterior part of
8 - передняя лопасть ноги. foot.
ASTEROPHILA JAPONICA 161
велигеры свободно плавают в жидкости псевдопаллиальной полости.
Выпускание личинок наружу через отверстие ложной мантии, вероятно,
производится поодиночке.
1. Внешний вид
Рисунки 43 Аи Б передают внешний вид сформированной личинки.
Тело личинки поделено на три отдела: голову, ногу и внутренностный
мешок.
Голова плоло отграничена от остального туловища. На передней
поверхности она несет пару коротких округлых щупалец (2), имеющих
сравнительно крупные размеры. Позади них находится парус (1), со-
стоящий из двух уховидных, не соединяющихся друг с другом лопастей,
очень нежных и прозрачных. Каждая лопасть по периферии ограничена,
непрозрачной белой каемкой высокого эпителия, который несет длин-
ные и грубые реснички, уменьшающиеся в размерах по направлению от
середины к краям.
Между щупальцами и ногой на небольшом возвышении лежит хоро-
шо заметное снаружи ротовое отверстие (3).
Нога /рис. 43/ глубокой поперечной складкой разделена на два
отдела: передний (8) и залний (5) - и несет крышечку (6).
При рассматривании личинки со стороны устья раковины виден
широкий вход в объемистую мантийную полость /рис. 43 A.
Сквозь тонкую раковину частично просвечивает внутренностный
мешок, однако детали его строения удается рассмотреть только после
растворения раковины путем декальцинации слабо подкисленным спир-
том /рис. 45 A, B /. Сохраняющаяся при этом очень тонкая пленочка
органического вещества не мешает наблюдению.
Передняя часть внутренностного мешка прикрыта снаружи мантией
(4), различные участки которой вследствие неравномерной толщины
обладают неодинаковой прозрачностью. С правой стороны тела мантия
толста и делает невидимыми лежащие под ней органы; с левой стороны
/рис. 45, А /. непрозрачны лишь два участка, выделяющиеся белыми
матовыми пятнами на ŸOHE нежной стенки этого органа. Первый, He-
большой участок, округлых очертаний, соответствует супраинтести-
нальному ганглию (3), расположенному на потолке мантийной полости,
около ее вентрального края. Другой участок (5), серповидной Формы,
начинается в виде узкой полоски в глубине мантийной полости и далее,
загибаясь вперед и постепенно расширяясь, тянется до самого входа
в нее. Непрозрачность его объясняется тем, что по внутренней по-
верхности мантии проходит ресничная полоска, образованная высоким
мерцательным эпителием. Остальная часть мантии с левой стороны
прозрачна, и сквозь нее просвечивает задняя часть эктодермальной
кишки.
Вершина раковины занята эктодермальной средней кишкой (7), ко-
торая отчетливо заметна, благодаря большому количеству содержащих-
ся в ней нерассосавшихся желточных зерен, имеющих характерный жел-
то-оранжевый цвет. На правой стороне тела, в месте, соответствую-
щем концу шовной линии раковины, на фоне кишки выделяется белый
овальный половой зачаток /рис. 45 Б. (10). Несколько впереди рас-
сматриваемого участка энтодермальная кишка соприкасается с эктодер-
162
UCA
AG ul
Pie, 45:
EH. РРУЗОВ
0-25mm A
д =
с вершины раковины;
Раковина личинки.
вид
Б - вид со стороны устья.
1 - шовная линия;
а Viel bes
3 - париетальная мозоль.
Aslerophila japonica.
FIG. 45. Личинка с декальцинирован:
ной раковиной. А - вид
слева, Б - со спинной
стороны.
1 - парус; 2 - раковина;
3 - супраинтестинальный
ганглий; 4 - мантия;
5 - ресничная борозда
мантийной полости;
6 - перикардий; 7 - энто-
дермальная кишка;
8 - нога; 9 - щупальце;
О:25тт В
Larval shell. A, apical view; В,
apertural view. 1- suture; 2-
aperture; 3 - parietal calius.
10 - половой зачаток;
11 - почка.
Asterophila japonica. Larva with
decalcified shell. A, left side; В,
dorsal view. 1- velar lobe; 2-
shell; 3- supraintestinal ganglion;
4 - mantle; 5 - ciliated groove of
mantle cavity; 6- pericardium;
7 - entodermal gut; 8 - foot; 9 -
tentacles; 10 - gonadal rudiment;
11 - kidney.
ASTEROPHILA JAPONICA 163
мальной, и здесь же проходит задняя граница мантийной полости. В
непосредственном соседстве с последней, на спинной стороне тела, на-
ходятся зачатки почки (11) и перикардия (6) с сердцем, слабо про-
свечивающим сквозь его стенки. Почка лежит несколько впереди и ле-
вее сердца.
По словам А. В. Иванова, наблюдавшего личинок А. japonica
в живом состоянии, большая часть их тела бесцветна и только верши-
на внутренностного мешка окрашена в желто-оранжевый цвет вследствие
наличия в ней желточных зерен.
2. Раковина и крышечка.
Низкая выпуклая раковина личинки, изображенная на рис. 44 А,Б,
асимметрична и геликоидно закручена вправо. Весь ее завиток обра-
зует немногим более одного оборота, вследствие чего мягко закруг-
ленная вершина (арех) располагается недалеко от устья, и высота ра-
ковины оказывается меньше ее ширины. На верхней поверхности рако-
вины заметна неглубокая короткая шовная линия (1).
Устье /puc. 44, B (2)/ имеет в общем овальную Форму, но на
участке, прилегающем к начальному обороту завитка, TAM, где Hapyx-
ная губа устья переходит во внутреннюю, образуется сглаженный у
вершины апикальный угол. Перистом на рассматриваемом участке обра-
зует небольшую париетальную мозоль (3). Края устья несколько отог-
нуты наружу.
Высота раковины колеблется от O, 27 мм до O, 31 мм, наибольшая
ширина равна O, 57 MM.
Крышечка, расположенная на задней лопасти ноги, в общем повто-
ряет Форму устья. Она состоит из рогоподобного вещества, сохраняет-
ся при кислых фиксациях, совершенно прозрачна, имеет мелкую попереч-
ную исчерченность и обычно плохо заметна.
По Форме раковина личинки Asterophila чрезвычайно сходна с
таковой Entocolax schwanwitschi (Schwanwitsch, 1917). Она
также напоминает раковину только что вылупившихся личинок Balcis
alba, В. devians и Pelseneeria stylifera (=Stilifer stylifer),
описанных Лебур ( Lebour, 1932, 1935) и Торсоном (Thorson, 1946).
Однако поздние личиночные стадии этих моллюсков уже существенно
отличаются от личинок Asterophila тем, что их раковина приобре-
тает башневидную Форму и имеет около пяти оборотов. Личинки А.
japonica вплоть до начала метаморфоза сохраняют раковину, свой-
ственную ранним велигерам. Стадия, соответствующая позднему вели-
repy Melanellidae, вымала из онтогенеза исследуемой формы.
3. Нога и педальные железы. Колюмеллярный мускул.
Нога личинки Asterophila представляет самый мускулистый ор-
ган тела. Помимо собственной мускулатуры, она содержит волокна,
прекрасно развитого колюмеллярного мускула /puc. 46/, который сво-
им задним концом прикрепляется к столбику раковины, а спереди, за-
гибаясь в соответствии со спиральной закрученностью внутренностно-
го мешка, входит в толщу соединительной ткани ноги позади педаль-
BE... EFYS0B
Puc. 46. Сагиттальный разрез через личинку. Маллори.
FIG. 46. 1 - парус; 2 - церебральный ганглий; 3 - плевральный
ганглий; 4 - эпителий внутренностного мешка; 5 - ман-
тия; 6 - эктодермальная кишка; 7 - мантийная железа;
8 - мантийная полость; 9 - сердце; 10 - раковина;
11 - перикардий; 12 - энтодермальная кишка; 13 - жел-
точные зерна; 14 - соединительная ткань; 15 - колю-
меллярный мускул; 16 - крышечка; 17 - задняя лопасть
ноги; 18 - эпителий ноги; 19 - отверстие подошвенной
железы; 20 - железистые клетки; 21 - передняя лопасть
ноги; 22 - педальный ганглий; 23 - отверстие краевой
железы; 24 - щупальце; 25 - краевая железа; 26 - по-
дошвенная железа.
Sagittal section through larva. Stained with Mallory’s. 1 - velar lobe; 2 - cerebral
ganglion; 3- pleural ganglion; 4- epithelium of visceral mass; 5 - mantle; 6 -
ectodermal gut; 7 - pallial gland; 8 - mantle cavity; 9- heart; 10 - shell; 11-
pericardium; 12 - entodermal gut; 13 - yolk granules; 14 - connective tissue; 15 -
columellar muscle; 16 - operculum; 17 - posterior part of foot; 18 - epithelium of
foot; 19 - opening of gland of sole; 20 - glandular cells; 21 - anterior part of foot;
22 - pedal ganglion; 23 - opening of glandular area; 24 - tentacle; 25 - glandular
area; 26 - gland of sole.
ного ганглия. Здесь OH разбивается на два равных пучка, один из
которых подходит к задней, несущей оперкулюм, стороне ноги, а дру-
гой проходит между педальными железами к ее брюшной поверхности,
соответствующей ползательной подошве других моллюсков. Сокраще-
нием колюмеллярного мускула личинка может втягиваться внутрь рако-
вины и прикрывать устье крышечкой, причем действие переднего пуч-
ка мускульных волокон вызывает складывание ноги попалам и появле-
ASTEROPHILA JAPONICA 165
ние глубокой поперечной щели, делящей ногу на две лопасти.
Передняя лопасть ноги имеет овальные очертания и очень выпук-
ла /рис. 46 (21)/. Ee длина примерно в два раза меньше ширины.
На границе этой лопасти с головой, на медиальной линии тела, нахо-
дится небольшое отверстие передней педальной железы (23).
Вторая лопасть более массивная, прямоугольная, со слегка за-
кругленным задним краем и уплощенной брюшной поверхностью. Ee сво-
бодная спинная сторона, которая при складывании ноги обращена назад,
несет operculum. В толще этого отдела залегает задняя педальная
железа /рис. 46 /, открывающаяся широким отверстием на линии пере-
гиба ноги (19).
Вся поверхность ноги, за исключением оперкулярной области,
покрыта мерцательным цилиндрическим эпителием обычного строения.
На подошве среди мерцательных клеток встречаются отдельные крупные
железистые клетки, строение которых рассматривается ниже.
Эпителий оперкулярной области невысокий, почти кубический,
нерезко переходит в плоский эпителий брюшной поверхности внутрен-
ностного мешка. Железистые и мерцательные элементы в нем отсут-
ствуют.
Большая часть ноги занята педальными железами.
Наружное отверстие передней железы ведет в короткий, неширо-
кий канал, образованный впячиванием покровов, которые в рассматри-
ваемом участке состоят из кубического или плоского мерцательного
эпителия. На задней стенке канала клетки несколько выше, чем на
передней, и реснички на них развиты лучше /рис. 47 (23) /. Часто
на передней стенке реснички вовсе отсутствуют.
Канал направляется косо назад и в самой глубине его клетки
испытывают железистое перерождение: размеры их резко возрастают,
а базальные концы расширяются и погружаются в толщу ноги и головной
лопасти. Замечательно, что все железистые клетки располагаются
по одну сторону канала - черта, свойственная взрослым моллюскам
Stiliferidae. Эти клетки образуют компактную массу и, благо-
даря этому, сильно деформируются. Их расширенные базальные концы
содержат интенсивно окрашивающиеся, богатые хроматином ядра, от-
тесненные к периферии железы /рис. 47 /. У многих особей железа,
переполнена зернистым секретом, имеющим слизистую природу и мета-
хроматически окрашивающимся гематоксилином в фиолетовый цвет /рис.
47 (25)/. Кроме того, в протоплазме присутствует несколько круп-
ных округлых вакуолей, содержимое которых вымывалось при обработ-
ке препарата. Плазма клеток слегка окрашивается бисмаркбрауном,
что указывает на присутствие слизи, равномерно распределенной в
клетке.
Вторая педальная железа /рис. 46 (26)/, примерно такой же
величины, что и первая, располагается непосредственно позади нее.
По ее передней и задней поверхностям тянутся волокна колюмелляр-
ного мускула. Она также является производной покровного эпителия
ноги и образована инвагинацией части’ клеток вглубь тела личинки.
На рис. 46 (19) отчетливо видна щель впячивания.
Неправильной формы железистые клетки имеют очень большие
размеры. Так же как у клеток передней железы, их базальные концы
расширены и содержат чрезвычайно деформированные ядра, оттесненные
к периферии /рис. 46/. Специальный выводной канал отсутствует.
166
ных зерен. Сами реснички могут отсутствовать.
Протоплазма наполнена неоформленным секретом слизистой приро-
ды. Он интенсивно окрашивается бисмаркбрауном и по Маллори, но
герматоксилин не воспринимает. Многочисленные вакуоли не содер-
жат видимого секрета.
Без резких границ железистое впячивание переходит в эпителий
подошвы. По периферии отверстия железы, среди мерцательных кле-
ток покровов присутствуют отдельные крупные железистые клетки
/рис. 46 (20)/, отличающиеся от клеток железистого впячивания 1
только меньшими размерами и тем, что их ядра почти не деформиро- }
ваны. Клетки открываются наружу в промежутках между ресничными |
клетками. В переднем отделе ноги подобные клетки расположены гу-
ще, чем в заднем.
Судя по расположению, структуре и характеру секрета, железа
соответствует подошвенной железе Melanellidae и других брюхо- |
HOTUX моллюсков.
Подобную железу имеют личинки всех исследованных Entoconch-
idae и Paedophoropodidae. Личинки Melanellidae и Stilifer-
idae, к сожалению, остаются до сих пор He изученными.
Е РОВ
Под наружной поверхностью клеток находится слой базальных реснич-
|
5
4. Мантия
Хорошо развитая мантийная полость доходит почти до вершины
внутренностного мешка и слегка асимметрична. Мантийная складка,
/рис. 46 (5)/ состоит из двух слоев эпителия, переходящих по краю
один в другой. Наружный прилегает к раковине и образован крайне
уплощенными клетками с чешуевидными ядрами. Сзади он переходит
в такой же эпителий внутренностного мешка.
Правая сторона мантийной складки дифференцирована в виде ман-
тийной железы (7), образованной клетками двух родов. Одни из них
невысокие, цилиндрические, лишенные ресничек, с протоплазмой, со-
держащей множество мелких прозрачных вакуолей. У отдельных, глав-
ным образом, молодых экземпляров внутри вакулей можно наблюдать
массу капель или зерен секрета, который после сулемовых фиксаций
и окраски железным гематоксилином с лихтгрюном приобретает глубо-
кий зеленовато-серый цвет. Клетки этого сорта располагаются в са-
мой глубине мантийной полости. Ближе к выходу из нее подобные
клетки сменяются другими, тоже железистыми и лишенными ресничек, но
с гомогенным секретом, собранным внутри одной-двух (реже трех) круп-
ных вакуолей. После окраски азокармином по Гейденгайну секрет
приобретает светло-желтый или розоватый оттенок, а железный гема-
токсилин им почти не воспринимается.
У самого края мантии располагаются низкие клетки, лишенные сек-
реторной функции.
Приблизительно по медиальной линии мантии проходит ресничная
полоска /рис. 45 А (5)/, отделяющая мантийную железу от правого
прозрачного района мантии. Мерцательные клетки кубические, с длин-
ными ресничками и хорошо развитыми базальными зернами /рис. 48 (26)/.
Между обоими слоями мантийного эпителия могут присутствовать
редкие, рыхло лежащие соединительнотканные клетки, хотя обычно оба
ASTEROPHILA JAPONICA 167
O-Imm
Рис. 47. Сагиттальный разрез ue-
FIG. 47. рез личинку. Маллори.
26.— статоциет; el -WIOU- Sagittal section through larva.
ка; 28 - подошвенная же- Stained with Mallory’s. 26- sta-
леза; 29 - ротовое отверстие; tocyst; 27- kidney; 28 - gland
остальные обозначения как of sole; 29 - opening of mouth.
Ha puc. 46. Other numbers as in Fig. 46.
слоя TECHO сближены. Кровеносные лакуны развиты незначительно.
5. Кишечник
Расположенное на вершине небольшого возвышения головы ротовое
отверстие ведет прямо в полость эктодермальной передней кишки, ко-
торая представляет неширокую трубку, имеющую на всем протяжении
одинаковое строение и не разделенную на отделы. Задний конец киш-
ки образует слепо замкнутый мешок, входящий в завиток внутренност-
ного мешка и прилегающий к энтодермальному отделу кишечника.
Стенки кишки состоят из невысокого цилиндрического, лишенного
ресничек эпителия с крупными овальными ядрами /рис. 46 (6) /. Ка-
кие-либо железистые участки и отдельные железистые клетки во всем
эпителии отсутствуют. Протоплазма клеток гомогенная и не содержит
включений. Полость кишки лишена пищевого KoMKa.
Замкнутая с обоих концов средняя кишка энтодермального проис-
хождения /рис. 46-48 (12)/ занимает всю вершину внутренностного
мешка. Просвет кишки очень невелик. Стенки образованы крупными
клетками с неровными границами и чрезвычайно прозрачной плазмой.
Круглые или овальные ядра с ядрышком обычно оттеснены к периферии,
поскольку вся протоплазма наполнена нерассосавшимися желточными
зернами.
EH. MPYSOB
Задней кишки и анального отверстия HET.
По строению кишечника личинка Asterophila не отличается от
известных личинок Entoconchidae (Schwanwitsch, 1917; Иванов, 1953;
и др.), a также Paedophoropodidae (Ivanov, 1937).
Кишечник личинок Melanellidae имеет, вероятно, более слож-
ное строение ( Thorson, 1946).
6. Перикардий и сердце
В заднем отделе внутренностного мешка, на границе передней и
средней кишок, находится перикардий с зачатком сердца.
Эпителиальные стенки перикардия образованы чрезвычайно упло-
щенными клетками, столь тесно прижатыми к покровам внутренностного
мешка и пограничным органам, что по большей части делаются неви-
димыми.
Небольшая перикардиальная полость содержит трубковидный 3aua-
ток сердца, пересекающий ее от спинной стенки до брюшной. В сред-
ней части трубка имеет легкую перетяжку, а оба конца ее вздуты и
соответствуют предсердию и желудочку /рис. 46 (9)/. Мускульные
волокна в стенке сердца отсутствуют.
Мне не удалось обнаружить никаких сосудов, связанных с серд-
цем; по-видимому, их нет. Но в различных районах тела между клет-
ками соединительной ткани сохраняются полости кровеносных синусов
или лакун. Значительного развития они, впрочем, тоже не получают.
У всех изученных личинок Entoconchidae и Paedophoropodidae
нет ни перикардия, ни сердца. Сведения о личинках Stiliferidae
и Melanellidae отсутствуют.
1. TOURS
Рядом с перикардием на спинной стороне тела лежит небольшой
пузыревидный орган, стенки которого состоят из одного ряда клеток,
ограниченных снаружи тонкой мембраной /рис. 47 (27)/. Дистальные
концы клеток языками вдаются в полость органа. Округлые ядра за-
нимают центральное положение или слегка прижаты к базальной мем-
бране. Грубозернистая протополазма содержит многочисленные вакуо-
ли, лишенные конкреций. С левой стороны орган вплотную примыкает
к перикардию, но не соединяется с ним. Положение, форма и строе-
ние органа не оставляют сомнения в том, что это - зачаток почки.
Выделительное отверстие отсутствует.
Интересно, что у личинки Paedophoropus dicoelobius иванов (Ivanov,
1937) встретил орган, сходно расположенный в левой части внутрен-
ностного мешка. Этот орган в существенных чертах напоминает почку
личинки нашего моллюска, чем подтверждается предположение Иванова,
о природе данного образования.
У личинок всех Entoconchidae зачаток почки отсутствует.
8. Нервная система,
В переднем отделе личинки, под эктодермальной кишкой, распо-
ASTEROPHILA JAPONICA 169
лагаются три пары TECHO сближенных ганглиев /puc. 46 (2, 3, 22)/.
Самые крупные из них, церебральные (2), лежат впереди и ox-
ватывают кишку с боков. OT каждого из них вперед к щупальцам отхо-
дит тяж нервных клеток, сопровождающих нервные волокна, заходящие
в щупалвце. Сзади церебральные ганглии соединяются с небольшими
плевральными (3). Под этими ганглиями, заходя нижними концами в
ткани ноги, располагается пара педальных ганглиев (22), соединенных
друг с другом короткой комиссурой. К их задней поверхности приле-
гают статоцисты /рис. 47 (26)/. Педальные ганглии при помощи це-
ребро- педальных коннективов связаны с церебральными, а посредст-
вом другой пары коннективов (плевро-педальных) - с плевральными
ганглиями. Оба коннектива столь коротки и толсты, что, вероятно,
было бы правильнее говорить о слиянии ганглиев в общую массу /рис.
Aegean (2. 3, 122) И
Последний, непарный ганглий /рис. 48 (28) / лежит на левой
стороне тела, внутри мантийной складки около ее основания. Он
имеет приблизительно округлую Форму, невелик и не соединяется с
передней частью центральной нервной системы. Его положение воз-
ле перикардия соответствует положению супраинтестинального ганглия
y взрослых форм, хотя там он находится целиком во внутренностном
мешке, не заходя в мантию. По-видимому, это обстоятельство объяс-
няется сильной редукцией мантийной складки у взрослых женских осо-
бей Asterophila.
Органы чувств представлены парой небольших округлых щупалец
и статоцистами с единственным статолитом. Глаза отсутствуют.
Центральная нервная система личинок всех изученных паразити-
ческих брюхоногих не подверглась существенным изменениям. В ином
‘ положении оказываются органы чувств. У личинок примитивных моллюс-
ков, вроде Balcis alba, В. devians и Pelseneeria stylifera,
имеются хорошо выраженные, заостренные Ha конце щупальца, Ha расши-
Рис. 48. Поперечный разрез через
FIG. 48. личинку на уровне поло-
вого зачатка. Кислый ге-
малаун Мейера, лихтгрюн.
26 - ресничная борозда
мантийной попости; 27 -
половой зачаток; 28 -
супраинтестинальный
ганглий. Остальные обоз-
начения как на рис. 46.
Anterior sectionthrough larva at
the level of the gonadal rudiment.
Stained with Mayer’s acid haema-
lum, light green. 26 - ciliated
groove of mantle cavity; 27- go-
nadal rudiment. 28- supraintes-
tinal ganglion. Other numbers
as in Fig. 46.
170 EX. TEYSOB
ренных базальных частях которых располагаются глаза ( Lebour,
1932, 1935; Thorson, 1946). У личинок Paedophoropodidae
и низших Entoconchidae щупальца в значительной мере упрощены, a
глаза вовсе отсутствуют ( (Ivanov, 1937; Иванов, 1953; Schwanwitsch,
ISE
Наконец, y личинок Ратещетохепо$ нет ни щупалец, ни глаз
(Иванов, 1949). У Parenteroxenos исчезают также и статоцисты,
присутствующие у личинок всех остальных паразитических брюхоногих.
9. Половой зачаток.
В вершине внутренностного мешка на уровне конца шовной линии
раковины располагается половой зачаток. Он находится на правой
стороне тела, непосредственно под покровами, соприкасается с энто-
дермальной кишкой /рис. 48 (27)/ и представляет собой лепешковид-
ное образование, состоящее из крупных, недифференцированных клеток
с большими округлыми ядрами, каждое из которых содержит по единст-
венному ядрышку. Протоплазма клеток окрашивается гематоксилином. |
В общем, половой зачаток Asterophila очень напоминает соот-
ветствующие органы личинок Entocolax schwanwitschi, Е. rimsky-
korsakovi, Paedophoropus и Parenteroxenos (Schwanwitsch,
1917; Ivanov, 1937; Иванов, 1949 a, 1953). Сведения о половом
зачатке личинок Melanellidae и Stiliferidae отсутствуют.
Подводя итоги, можно сказать, что по уровню организации ли-
чинка Asterophila стоит ближе всего к личинкам примитивных
Entoconchidae. Однако отдельные черты ее строения, и, в первую
очередь, присутствие рудиментов перикардия и почки, свидетельству-
ют о большей примитивности исследуемой формы.
Сравнение с личинками Melanellidae и Stiliferidae
крайне затруднено из-за их плохой изученности. Однако имеющиеся
данные позволяют заключить, что личинки Asterophila во многом.
упрощены по сравнению с личинками примитивных паразитических брю-
хоногих. В филогенезе подобное упрощение, вероятно, происходило
как путем редукции определенных органов, т.е. полного исчезновения
каких-либо их зачатков, так и путем отрицательной анаболии (Беуег-
cov , 1931), т.е. выпадения конечных стадий развития. Отсутствие
глаз у личинки нашего вида, по всей вероятности, есть следствие
первого процесса; рудиментарный характер раковины, щупалец и не-
которых других образований - результат недоразвития соответствую-
щих органов.
rte D EE
У. Систематическое положение Asterophila u ee филогенети-
ческие взаимоотношения с другими паразитическими брюхоногими
Во всей организации А. japonica наблюдается сочетание при-
митивных, унаследованных от отдаленных предков черт строения с
признаками далеко идущей специализации. Интересно проанализиро-
вать строение животного под этим углом зрения.
К числу признаков первой категории относятся: расчленение
тела на голову, внутренностный мешок и ногу; присутствие у некото-
ASTEROPHILA JAPONICA 21
рых экземпляров рудимента хобота; наличие рудимента ноги; сохране-
ние рудиментарной мантии, расположенной на левой стороне тела; нор-
мальное развитие перикардия с двукамерным сердцем; наличие почки и
ее положение рядом с перикардием, расположение почечных трабекул
исключительно на наружной стороне органа; строение нервной системы
и наличие хиастоневрии; раздельнополость, строение половой системы,
открывающейся наружу щелевидным половым отверстием, положение со-
вокупительного органа справа от ноги; откладка яиц в коконах; ор-
ганизация личинок, обладающих спирально закрученной дексиотропной
раковиной.
Вторая категория признаков: наличие ложной мантии головного
происхождения; редукция головы, глаз и щупалец; отсутствие хобота
у некоторых экземпляров и сильная его редукция у остальных; руди-
ментарный характер ноги, лишенной крышечки и педальных желез; утра-
та раковины и спиральной закрученности внутренностного мешка; ре-
дукция мантии и мантийной полости, исчезновение жабры, осфрадия и
гипобранхиальной железы; утрата колюмеллярного мускула и редукция
мускулатуры тела; субституция желудка печенью и ее смещение в се-
редину внутренностного мешка, исчезновение задних отделов кишечни-
ка; смещение перикардия на брюшную сторону, положение предсердия
впереди желудочка; резкий половой диморфизм, прикрепление самцов
к Псевдопаллиуму самок; вынашивание яиц под защитой ложной мантии.
Многие из примитивных признаков указывают на положение Astero-
phila 5 пределах Prosobranchia Monotocardia, в частности
среди Taenioglossa. Известно, что паразитизм внутри этого от-
ряда возникал многократно и независимо друг от друга. В настоящее
время известно (если не считать саму Asterophila ) шесть групп
паразитических моллюсков, берущих начало от разных семейств свобод-
ноживущих брюхоногих (Ivanov , 1937; Иванов, 1941): Capulidae,
Pseudosacculidae, Ctenosculidae, паразитические Pyramidellidae,
паразитические Melanellidae - Stiliferidae - Entoconchidae,
происходящие OT свободноживущих Melanellidae, и Paedophoropodidae,
происходящие также oT Melanellidae.
Последние три группы вместе со свободноживущими Aclididae
Тиле (Thiele, 1929) относит к трибе Aglossa.
Попытаемся теперь сравнить Asterophila с паразитическими
моллюсками, т. к. его родственные связи естественно искать именно
здесь. При этом Pseudosacculidae и Ctenosculidae сразу выпадут
из круга рассматриваемых форм, т.к. ряд глубоких различий разобща-
ет их с Asterophila (Heath, 1910; Hirase, 1927).
Нельзя сближать наш вид также с паразитическими Capulidae,
несмотря на ряд общих черт их строения, поскольку сходство распро-
страняется либо на признаки, вообще часто встречающиеся среди
Prosobranchia (концентрация нервной системы; строение полового
аппарата), либо на признаки, конвергентно возникакщие у многих па-
разитов (ложная мантия, редукция пищеварительной системы и др.).
Некоторые черты строения Asterophila, бесспорно унаследо-
ванные ею от своих предков, резко отличают ее от СариПаае.
Наиболее важным является, пожалуй, положение совокупительного ор-
гана самцов A.japonica на правой стороне тела, в то время как y
Thyca он расположен слева от ноги. Положение мантии Asterophila
на левой стороне тела также отличает ее от Capulidae (Adam, 1933, 1934).
172 E. H. ГРУЗОВ
Прежде чем перейти к сравнению Asterophila с паразитически-
ми моллюсками трибы Aglossa, остановимся вкратце на взаимоотно-
шениях между представителями этой группы. В анатомическом отноше-
нии все относящиеся сюда семейства, за исключением Pyramidellidae,
нечетко отграничены друг от друга. В особенности это касается
семейства Melanellidae и Stiliferidae, морфологические отли-
чия между которыми попросту отсутствуют. По степени развития лож-
ной мантии, редукции ноги, изменениям в пищеварительной системе и
концентрации нервной системы различные представители Melanellidae
часто оказываются более специализированными, чем примитивные
Stiliferidae. Строение остальных органов, по-видимому, одинаково в
обоих семействах.
Также и конхиологический критерий оказывается недостаточным
для разделения Melanellidae и Stiliferidae, на что указывал
еще Нирштрас ( Nierstrasz, 1913). Естественно поэтому объединять
всех представителей рассматриваемых семейств в одно семейство
Melanellidae.
Едва ли заслуживают выделение в отдельное семейство виды
Pelseneeria. Единственное отличие этих животных от Melanellidae
касается природы ложной мантии, представляющей у Melanellidae
разрастание покровов головы, a у Pelseneeriidae - ноги. Однако
разнообразие строения истинных Melanellidae касается не менее
важных признаков, а Филогенетическая неоднородность этого семейст-
ва так велика, что позволяет включить в Hero и Pelseneeria.
В частности, y Stilifer celebensis Y Megadenus arrhynchus
нога претерпевает существенную перестройку в связи с приспособле-
нием к новым функциям /Hirase, 193247
B Melanellidae s. lat. можно включить и Paedophoropodidae,
описанное Ивановым (Ivanov, 1937) после исследования единственного
вида Paedophoropus dicoelobius. Главным его отличием oT Stiliferidae
автор считает отсутствие ложной мантии головного происхождения,
своеобразное строение ноги и отсутствие резкого полового диморфиз-
ма. Однако описанная позднее (Грузов, 1957) Molpadicola orient-
alis в известной мере заполняет пробел между Paedophoropodidae
и Melanellidae. Строение ноги этой формы, дифференцированной
на центральную часть с ползательной подошвой и боковые лопасти,
позволяет видеть примитивное состояние этого органа. Боковые ло-
пасти по форме напоминают ложную мантию Pelseneeria и имеют
одинаковую с ней педальную природу. Сильная специализация ноги
Paedophoropus стоит в связи с превращением ее в инкубационный
орган.
Не следует придавать также слишком большое значение слабой
редукции самцов относительно самок. Известное несоответствие меж-
ду уровнем общей редукции животного и степенью полового диморфФиз-
ма наблюдается, по-видимому, и у Stiliferidae. Таким образом,
различия между Paedophoropodidae и Melanellidae не столь Cy”
щественны, чтобы противопоставлять их друг другу в систематичес-
ком отношении.
Эволюция Paedophoropodidae, как и Pelseneeriidae
происходила, конечно, особым путем, однако и Stiliferidae не
представляют однородной группы. Помимо типичных видов, эволюция
которых шла от свободноживущих форм через эктопаразитов к эндопа-
A En ae
ASTEROPHILA JAPONICA 173
разитическим Entoconchidae, семейство Stiliferidae включает
в себя также такие формы, как Mucronalia variabilis и Рата-
stilifer, которые занимают совершенно обособленное положение и, ве-
роятно, независимо происходят от свободноживущих моллюсков, близ-
ких к современным Melanellidae (Иванов, 1952). Типичные
Stiliferidae (Mucronalia, Megadenus, Stilifer и Gasterosiphon)
также не представляют единой линии развития, хотя их различия He
столь существенные (Nierstrasz, 1913).
Таким образом, моллюски, происходящие от Melanellidae,
образуют целый пучок Форм, расходящийся в разные стороны. При
этом различия крайних членов разных эволюционных направлений ока-
зываются иногда весьма существенны. Однако эти формы через прими-
тивных представителей связаны друг с другом, и поэтому деление груп-
пы на ряд семейств кажется нам недостаточно обоснованным. Гораздо
естественнее в настоящее время относить их к одному обширному се-
мейству, за которым лучше всего сохранить название Melanellidae.
К этому семейству тесно примыкает Entoconchidae, представляющее
собой наиболее ‘деградированных паразитических гастропод. Несмотря
на то, что филогенетическая связь обоих семейств не вызывает ника-
ких сомнений, оснований для объединения их воедино пока что недо-
статочно. Правда, можно надеяться, что новые находки окончательно
заполнят пробел между этими группами.
Сходство А. japonica c представителями Melanellidae и
Entoconchidae подчеркивалось на протяжении всей работы. OHO pac-
пространяется прежде всего на признаки, унаследованные от свободно-
подвижных предков, такие как состав центральной нервной системы,
строение почки и полового аппарата и, особенно, организация личин-
ки Asterophila.
Далее, процессы редукции органов у A.japonica и Melanellidae
протекают сходным образом: раковина редуцируется, пищеваритель-
ная система упрощается и т. д. Даже такая своеобразная особен-
ность, как почти полное исчезновение хобота, встечается у
Megadenus arrhynchus.
Исчезновение спиральной закрученности внутренностного мешка
и связанное с этим смещение перикардия на брюшную сторону, а также
изменение в положении сердца сходным образом, хотя и конвергентно,
осуществлены у Paedophoropus и Molpadicola. Одинаково про-
исходила редукция мантийного комплекса органов, в результате чего
половое отверстие оказалось вынесенным за пределы мантийной полос-
ти. В то же время левый край половой щели у Asterophila лежит
y самого входа в мантийную полость, что до некоторой степени сбли-
жает е с примитивными Melanellidae.
Наконец, немногочисленные случаи прогрессивного развития от-
дельных органов (например ложной мантии) указывают на идентич-
ность и этих процессов у А. japonica и Melanellidae - Entoconch-
idae.
При таком положении вещей He имеет смысла сохранять самостоя-
тельность семейства Asterophilidae, как это было сделано Thiele
(1929) на основании данных Рандаль и Хиза. Если исходить из этих
данных, то наиболее замечательными особенностями строения Astero-
phila нужно было бы признать следующие: 1/ Положение перикардия
и почки на правой стороне тела, а гонодукта - на левой и 2/ нали-
174
E... : ГРУЗОВ
une рудиментов слюнных желез. Однако, как нам удалось показать,
топография’ мантийного комплекса у исследуемой формы не отличается
от нормы, присущей Taenioglossa. Что же касается слепых карма-
нов глотки, то бедность этих образований морфологическими призна-
ками не позволяет установить их гомологию со слюнными железами
других гастропод, и, следовательно, точка зрения Рандаль и Хиза
оказывается по меньшей мере недоказанной. Толкование природы этих
образований оказывается всецело зависящим от нашего понимания Qu-
логенетических связей Asterophila c другими моллюсками.
Все остальное строение нашего вида не выходит за пределы мно-
гообразия, наблюдаемого внутри Melanellidae. Поэтому нам ка-
жется правильнее относить А. japonica к этому семейству на правах
самостоятельного рода. При этом приходится признать, что диверти-
кулы глотки возникли у нее как новообразования в связи с переходом
к обитанию в новых условиях. Аналогичные образования передней час-
ти кишечника появились также у Megadenus holothuricola, М. voeltzkovi
и Entocolax rimsky-korsakovi.
Особенная близость обнаруживается между A.japonica и Mega-
denus arrhynchus. Так, обе рассматриваемые формы практически ли-
шены хобота, - особенность, указывающая на особый путь их эволюции.
Вместе с тем, Megadenus сохранил еще рудименты ретракторов хобота,
полностью исчезнувшие у нашего вида.
Другая характерная черта Megadenus состоит в неравномерном
развитии ложной мантии на правой и левой сторонах тела. Это объяс-
няется особенностями паразитирования данной Формы, сидящей как бы
боком в чашеобразном углублении стенки тела морской звезды. Наблю-
даемая у Asterophila неравномерность в развитии вентрального и
дорзального участков псевдопаллиума, выражающаяся в асимметричном
положении вторичного женского полового отверстия на брюшной стороне
ложной мантии, вероятно, вызвана аналогичными условиями паразити-
рования ее предков. В соответствии с меньшей специализацией
Megadenus, его ложная мантия развита значительно слабее, чем y Ha-
шего вида. Наиболее существенные различия во внешней морфологии
между сравниваемыми видами касаются формы внутренностного мешка,
степени развития мантии, мантийного комплекса органов и строения
ноги. Все перечисленные органы, кроме ноги, у Megadenus мало
отличаются от соответствующих образований у свободноживущих брюхо-
ногих. Нога испытывает прогрессивное развитие в связи с приобрете-
нием новой Функции обновления воды в мантийной naiocTu. У Astero-
phila эти органы подверглись сильной редукции, HO, тем не менее,
сохранили свое первоначальное положение.
Пищеварительная система рассматриваемых видов в принципе сход-
Ha, HO y Megadenus несколько примитивнее и открывается наружу
анальным отверстием. Желудок у обоих видов отсутствует, как, впро-
чем, и у большинства паразитических брюхоногих.
Сравнение кровеносной и выделительной систем Megadenus и
Asterophila He дает подтверждений их родства, хотя и не противо-
речит ему. Почка в обоих случаях несет трабекулы только на своей
наружной стороне и открывается почечным отверстием в глубине ман-
тийной полости.’ Редукция кровеносной системы зашла у А. japonica
дальше и привела к полному исчезновению сосудов, хорошо выраженных
у Megadenus arrhynchus.
ASTEROPHILA JAPONICA 175
Enteroxenos
Parenteroxenos
'
Entoconcha
Entocolax
Diacolax
(Entoconchidae)
Asterophila Paedophoropus'
|
Asterophilidae
Molpadicola
Gasterosiphon
Ah (Paedophoropodidae)
Stilifer
В Parastilifer р Odostomia
М. arrhynchus- —- Megadenus Mucrona lia/ Pelseneeria Turbonilla
(Pelseneeriidae) (Pyramidellidae)
Mucronalia variabilis
(Stiliferidae)
Melanella, Balcis n sp.
(Melanellidae)
Puc. 49. Схема Ффилогенетических взаимоотношений паразитиче-
FIG. 49. ских моллюсков трибы Aglossa.
Diagram of phylogenetic interrelations of parasitic mollusks of the tribe Aglossa.
Центральная нервная система М. arrhynchus состоит из тех
же ганглиев, что и у Asterophila, однако гораздо менее концен-
трирована. Плевральные ганглии вполне обособлены от церебральных.
Висцеральное кольцо замкнуто, хотя имеется только один висцераль-
ный ганглий. Много общего имеется в строении буккального отдела
нервной системы. Буккальные ганглии Megadenus соединяются при
помощи буккальной и лабиальной комиссур над и под кишкой. Имеется
пара мелких лабиальных ганглиев, возможно, гомологичных небольшим
нервным узелкам в глотке Asterophila.
Женская половая система сравниваемых видов одинаково харак-
теризуется наличием дополнительной белковой железы, несвойственной
большинству Melanellidae. Дополнительная железа сходного с
Asterophila строения имеется также и в составе мужского полового
аппарата Megadenus. Самцы обоих видов обладают совокупительным
органом, позволяющим им копулировать с самками, находясь на неко-
тором удалении от них, снаружи ложной мантии.
Из сказанного ясно, что М. arrhynchus по своей организации
должен быть весьма сходен с предками Asterophila, и в системе
паразитических гастропод эти формы необлодимо располагать побли-
зости друг от друга. Однако непосредственно выводить А. japonica
oT Megadenus невозможно, т.к. оба вида обладают чертами глубокой
специализации.
176 E. НЧ. ГРУЗОВ
Филогенетические взаимоотношения между моллюсками трибы
Aglossa можно представить в виде следующей схемы /рис. 49/. Вид-
но, что Asterophila есть представитель боковой ветви эволюцион-
ного ряда Melanellidae - Entoconchidae и филогенетически He
предшествует последним. Это доказывается наличием у не некото-
рых специфических особенностей, прежде всего, сильной редукцией
хобота и своеобразным строением ложной мантии: положение отверстия
псевдопаллиума у Asterophila не соответствует положению сифона,
У Entoconchidae. С этим, по-видимому, связано и другое существен-
ное различие между ними, а именно, меньшая редукция самцов у наше-
го вида. Близость отверстия в ложной мантии к первичному половому
отверстию позволяет самцам, прикрепленным к наружной поверхности
органа, копулировать с самками. У Entoconchidae отверстие сифо-
на помещается на заднем конце тела, и их самцы, вероятно, с самого
начала располагались во внутренней полости псевдопаллиума. Это
могло создать условия для их редукции и, в частности, для утраты
ими совокупительного органа.
Таким образом, сходство Asterophila с Entoconchidae не
представляет собой результата их непосредственного родства, а объяс-
няетсяих происхождением от общих предков и дальнейшей параллельной
эволюцией под влиянием сходных условий существования. Подобный
параллелизм - явление весьма частое у паразитических гастропод.
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ASTEROPHILA JAPONICA ит
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JONKER, A., 1916, Uber den Bau und die Verwandschaft der parasitischen
Gastropoden. Tijdschr. Ned. dierk. Vereen., (2), 15(1): 17-89.
KOEHLER, R., et VANEY, C., 1903, Entosiphon deimatis, nouveau Mollusque
parasite d’une Holothurie abissale. Rev. Suisse Zool., 11: 23-41.
et , 1912, Nouvelles formes des gastéropodes ecto-
parasites. Bull. sci. Fr. Belg., Paris, ser. 7, 46: 191-217.
LEBOUR, M., 1932, The eggs and early larvae of two commensal gastropods,
Stilifer stylifer and Odostomia eulimoides. J. mar. biol. Ass., 18:
117-122.
, 1935, The larval stages of Balcis alba and B. devians. J. mar.
biol. Ass., 19: 65-69.
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MANDAHL-BARTH, G., 1941, Thyonicola mortenseni п. gen., п. sp., eine
neue parasitische Schnecke. Vidensk. Medd. naturch. Foren.,
Köbenhavn, 104: 341-351.
, 1945-46, Diacolax cucumariae n. gen., n. sp., a new parasitic
snail. Vidensk. Medd. naturch. Foren. Kébenhavn, Bd. 109: 55-68.
MULLER, J., 1852, Uber die Erzeugung von Schnecken in Holothurien. Arch.
Anat. Physiol.: 1-37.
NIERSTRASZ, H., 1913, Die parasitische Gastropoden. Erg. Fortschr. Zool.,
3: 534-593.
RANDALL, J. et HEATH, H., 1912, Asterophila, a new genus of parasitic
gastropods. Biol. Bull. mar. biol. Lab. Woods Hole, 22: 98-106.
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Nouvelle-Caledonie. Bull. Mus. Hist. nat., Paris, ser. 2, 26: 109-
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Lund., N.F., Afd. 2, 6(4): 1-67.
SARASIN, P. et F., 1885, Ueber zwei parasitische Schnecken. Zool. Anz.,
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salistische Mollusken aus Holothurien. Voeltzkow Reise Ostafrica
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SCHIEMENZ, P., 1889, Parasitischen Schnecken. Biol. Centralbl., 9: 567-
574, 585-594.
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THIELE, J., 1929, Handbuch der systematischen Weichtierkunde. 1: 1-376.
THORSON, G., 1946, Reproduction and larval development of Danish marine
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VANEY, C., 1913, L’adaptation des Gastropodes au parasitisme. Bull. sci.
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, 1914, Morphologie comparée des Gastropodes parasites. IX-e
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ABSTRACT
THE ENDOPARASITIC MOLLUSK ASTEROPHILA JAPONICA
RANDALL AND HEATH (PROSOBRANCHIA: MELANELLIDAE)
AND ITS RELATION TO THE PARASITIC GASTROPODS
E. N. Grusov
The anatomy of the endoparasitic mollusk Asterophila japonica Randall &
Heath has undergone severe modifications in the process of adaptation to its
mode of life. Previous information aboutits anatomy is in many waysincorrect,
and its systematic position has been uncertain.
The mollusk lives inthe body wall of starfishes (Fig. 1) found along the
Asiatic coast of the Pacific ocean. On the surface of the female mollusks are
ASTEROPHILA JAPONICA
attached the tiny neotenic males (Figs. 3, 4B), whose structure has not been
studied previously.
All the main subdivisions of the gastropod body were found; head, visceral
mass, and foot (Figs. 6, 9), although these subdivisions were strongly masked.
The head lacks tentacles and eyes. In the female it is sometimes prolonged
into a snout (Fig. 3, 14A), but usually this structure has developed incompletely
(Fig. 2) or disappeared completely (Fig. 14B); in the males it is always absent
(Fig. 10). From the surface of the head has originated an enormously developed
pseudopallium (Fig. 5-4; Fig. 6-1) enclosing the visceral mass, foot, and an
extensive pseudopallial cavity, where in the females the eggs develop into
veligers. The cavity communicates externally through an opening on the ventral
side of the pseudopallium (Fig. 2-3; Fig. 5-2).
The foot (Figs. 6, 10, 22) is vestigial; it lacks operculum, pedal glands, and
creeping surface, and is nonfunctional. The male copulatory organ originates
on the right side of the foot (Figs. 9, 10). In immature males there is some-
times the vestige of an anterior pedal gland (Fig. 24-8).
The visceral mass (Figs. 7, 8, 9, 10) has lost the shell and acquired an al-
most spherical form; it does not retain traces of spiral coiling.
The mantle and mantle cavity are vestigial, although they have retained the
primitive position to the left of the foot (Fig. 6-8); Fig. 9-3). The complex of
pallial organs has been dispersed and mostly reduced. Only the kidney has
retained its normal position and opens into the mantle cavity. Ctenidium,
osphradium, hypobranchial gland, and rectum have disappeared. The pallial
oviduct opens outside the mantle cavity (Fig. 8-1) on the right side of the body.
The digestive system begins with the oral opening, leading into a muscular,
sucking pharynx that has 2 blind diverticula inthe frontal plane (Figs. 14A, B-12);
Randall and Heath (1912) interpreted these as vestigial salivary glands. On the
other hand they can be interpreted as new structures, absent in the ancestral
forms. Characteristically all Melanellidae - Entoconchidae, with which Astero-
phila japonica has much in common, lack salivary glands. The nature of the
pharyngeal diverticula of Asterophila cannot be resolved conclusively, and
therefore one or another interpretation of these structures should not be in-
volved in our evaluation of the systematic position of the animal.
The short, glandless esophagus (Fig. 25-4) connects the pharynx with the
blind digestive gland or liver (Fig. 25-2). Jaws, radula, and lower intestine
are absent.
The circulatory system has also undergone a remarkable secondary simpli-
fication, affecting mainly the vascular apparatus. The pericardium retains a
normal position on the left side of the body next to the kidney (Fig. 8-10; Fig.
10-6). A renopericardial opening is absent. The heart is two-chambered (Fig.
8-8, 9). The vessels have been replaced by a system of lacunae and sinuses
(Figs. 12, 13). The kidney is normally developed. Respiration takes place
through the surface of the pseudopallium.
The central nervous system has the following plan (Fig. 31): the cerebral and
pleural ganglia are fused, forming an extensive ganglionic mass (5, 15), lying
on the esophagus. Ventral to these ganglia are 2 pedal ganglia (9), lying next to
the base of the foot. There are a pair of statocysts (8). On the pharynx are 2
buccal ganglia (1), connected with each other by 2 commissures (2). Thevisceral
loop is incomplete. One of its portions consists of visceral (4) and subintestinal
(6) ganglia, connected tothe left part of the cerebro-pleural mass (16). The other
portion consists ofa single supraintestinal ganglion (12). There is chiastoneury.
The female reproductive system (Fig. 38) consists of ovary and oviduct,
differentiated distally into 3 parts: accessory gland (4), seminal receptacle, and
pallial oviduct. Adhering in a cocoon-like mass the eggs lie in the pseudopallial
cavity (Fig. 6).
179
180
E. Н. ГРУЗОВ
The testis (Fig. 36-1) is connected by the vas deferens to a terminal énlarge-
ment, the accessory gland (6).
The larva is a typical veliger with slightly reduced lobes (Figs. 43 to 48). In
contrast to the larva of Entoconchidae it has a pericardium and kidney.
The whole anatomy of Asterophila indicates its closeness to Melanellidae -
Entoconchidae, so that allocating it to an independent family Asterophilidae, as
did Thiele (1929), is hardly justified. The characters for dividing the Melanell-
idae into separate families Melanellidae, Stiliferidae, Pelseneeriidae and
Paedophoropodidae are also inadequate. It is more correct to unite them into a
single broad family, Melanellidae s. 1., where the form under investigation
‘certainly belongs also. Fig. 49 illustrates the phylogenetic interrelations be-
tween representatives of this group.
RESUMEN
ASTEROPHILA JAPONICA
La anatomia del molusco endoparasito Asterophila japonica Randall & Heath ha
sufrido severas modificaciones en el proceso de adaptación. La información previa
sobre su anatomia es muchas veces incorrecta y la posición sistemática incierta.
El molusco vive en las paredes del cuerpo de estrellas de mar (Fig. 1), en la costa
asiática del Pacífico. Adheridos superficialmente al las hembras se encuentran
machos nototenicos (Figs. 3, 4B), cuya estructura no habia sido aun estudiada.
Aunque no claramente distinguibles, pueden apreciarse las principales regiones
del cuerpo gastrópodo: cabeza, masa visceral y pié (Figs. 6, 9). En la cabeza faltan
los tentáculos y Ojos, y en la hembra esta se prolonga en una trompa (Fig. 3, 14A),
incompletamente desarrollada (Fig. 2), o que desaparece por completo (Fig. 14B); en
los machos esta siempre ausente (Fig. 10). De la superficie cefálica se origina un
enorme seudopalio (Fig. 5-4; Fig. 6-1), envolviendo la masa visceral, pié, y en la
extensa cavidad seudopalial de las hembras se desarrollan los huevos en larvas
veligeras. Esta cavidad se comunica al exterior por un orificio ventral (Fig. 2-3;
Fig. 5-2).
Del pié (Figs. 6, 10, 22) sólo hay vestigios; no tiene opérculo, glandula pedal ni
superficie de reptación, siendo inactivo. El órgano copulador masculino sale por el
lado derecho del pié (Figs. 9, 10). En machos inmaduros hay algunas vestigios de
una glandula pedal anterior (Fig. 24-8).
No poseen concha y la masa visceral es casi esférica, sin presentar rasgos de
arrollamiento (Figs. 7, 8, 9, 10).
Del manto y su cavidad sólo hay vagos rasgos, aunque ha retenido su primitiva
posición a la izquierda del pié (Fig. 6-8; Fig. 9-3). El complejo de órganos paleales
está disperso y reducido. 5010 el rifñión ha mantenido su posición normal y se abre
en la cavidad paleal. Branquias, osfradios, glandula hipobranquial y el recto han
desaparecido. El oviducto se abre al exterior sobre el lado derecho (Fig. 8-1).
La boca conduce a una faringe muscular, succionadora, con dos diverticulos ciegos
en el plano frontal (Figs. 14A, B-12); Randall € Heath interpretan esto como un
vestigio de glandulas salivares. Por otra parte también pueden interpretarse como
estructuras nuevas, ausente en las formas ancestrales. Todos los Melanellidae -
Entoconchidae con los cuales Asterophila japonica tiene mucho de común, se carac-
terizan por la falta de glandulas salivares. La naturaleza de los diverticulos faringeos
de Asterophila no puede resolverse conclusivamente, y su interpretación no debe
incluirse en valuaciones sistemáticas.
El esófago, corto y sin glandulas (Fig. 25-4) conecta la faringe con la glandula
digestiva ciega o hígado (Fig. 25-2). Mandibula, rádula e intestino inferior estan
ausentes.
El sistema circulatorio ofrece también una gran simplificación que afecta principal-
mente al aparato vascular. El pericardio tiene posición normal sobre la izquierda
cerca del hígado (Fig. 8-10; Fig. 10-6). Abertura renopericardial ausente. Corazón
ASTEROPHILA JAPONICA
con dos cämaras (Fig. 8-8, 9). Vasos remplazados por un sistema lacunar y senos
(Fig. 12-13). Riñón normal. Та respiracion se opera a traves del seudopalio.
El sistema nervioso tiene elplan siguiente (Fig. 31): ganglios cerebrales y pleurales
fusionados en una gran masa (5, 15) encima del esófago. En posición ventral a esos
ganglios hay 2 ganglios pedales (9), cerca de la base del pié. Hay un par de estatocistos
(8). Sobre la faringe hay dos ganglios bucales (1) conectados por comisuras (2). El
arco visceral es incompleto; una porción consiste de ganglios viscerales (4) y sub-
intestinales (6), conectados a la parte izquierda de la masa cerebro-pleural (16); la
otra porción consiste de un simple ganglio supraintestinal (12).
El sistema reproductor femenino (Fig. 38) consiste de ovario y oviducto diferenciado
distalmente en tres partes: glandulas accesorias (4), receptaculo seminal y oviducto
paleal. Masas ovigeras en forma de capullo yacen en la cavidad seudopalial (Fig. 6).
El testículo (Fig. 36-1) se conecta por el vas deferens a un terminal agrandado, la
glandula accesoria (6).
Larva veligera típica con lóbulos algo reducidos (Figs. 43 a 48), la cual, en contraste
con las de los Entoconchidae, tiene un riñón y pericardio.
La completa anatomía de Asterophila indica su afinidad con Melanellidae -
Entoconchidae, de modo que no justifica su ubicación por Thiele (1929), en una familia
diferente. Los caracteres que se han usado para dividir los Melanellidae, Stilliferidae,
Pelseneeridae y Paedophoropodidae son inadecuados. Es más correcta la unión en
una misma, amplia, familia Melanellidae, a la que pertenece la forma aquí investigada.
Figura 49 ilustra las relaciones filogenéticas entre los representates de este grupo.
181
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MATACOLOGTA, 1965, 3(2): 183-195
f
a36b:%
NE
SYMBIOTIC ERYCINACEAN BIVALVES LIBRARY,
Kenneth J. Boss VOU AV
Ichthyological Laboratory EU TS
Bureau of Commercial Fisheries, Fish and Wildlife Service UNIV Nal A
Department of the Interior, Washington 25, D. C., U.S. A.
ABSTRACT
This paper is a summary of the occurrence of symbiotic behavior among rep-
resentatives of the eulamellibranch superfamily Erycinacea.
Individual cases
of commensalistic, mutualistic, or even ectoparasitic and seemingly endopara-
sitic habits are presented and documentationis provided. The mollusks are dis-
cussed in relationto their hosts, and brief remarks are appended concerning the
general causal nature of these associations.
INTRODUCTION
During the preparation of a paper
on a bivalve living attached to the
stomatopod crustacean Lysiosquilla
(Boss, 1965), I had occasion to consult
the literature on commensal and para-
sitic lamellibranchs. The occurrence
of these bivalves is widely document-
ed in diverse publications, and it is
the primary purpose of this paper to
present a résumé of the scattered lit-
erature. In documenting the many known
examples of commensalism and para-
sitism in the Bivalvia, I have limited
the scope of this review to those in-
volving the eulamellibranch superfamily
Erycinacea. Cases of inquilinism, such
as mytilids inhabiting sponges and as-
Cidians or pectinids associated with
corals, examples of specialized boring
habits, such as Lithophaga or Clavagella
in corals, or instances of true
parasitism, such as the glochidium
in the Unionidae, have been omitted.
Further, no discussion of the defi-
nitions! of parasitism, mutualism, or
commensalism will be made since the
divisions among the phenomena are
arbitrary and commonly’ the exact
1Definitions of the terms relating to symbio-
tic phenomena may be found in Pennak (1964).
biological relationships between the
bivalve and its host or hosts are
unknown.
Most of the species of bivalves with
known patterns of commensal or para-
sitic behavior appear to have a high
degree of specificity. This specificity
may be illusory, occasioned by the lack
of detailed study or experimental ob-
servation. Thus, in a well-known spe-
cies, Mysella bidentata (Montagu),
range of hosts, including annelids, si-
punculids, and ophiuroids, has been docu-
mented, whereas in the majority of
Species only a single host has been
mentioned. The relationships between
the bivalves and their hosts are not
well known. It appears that the water
currents generated by the host are
usually utilized by the mollusk in feed-
ing. Further, some of the associa-
tions might well prove to be the means
of efficient dispersal for the mollusks.
In most examples it is difficult to detect
what benefit, if any, is derived by the
host animals.
Pelseneer (1909) has discussed the
evolution of 2 diverse phylogenetic
branches in the Erycinacea. The con-
chological studies of Chavan (1960) in-
clude a discussion of the evolution of
hinge mechanisms in the Erycinacea, and
considerations of anatomy have been
(183)
184 K. J. BOSS
presented by Pelseneer (1911), Kaspar
(1913), Popham (1939; 1940), and Old-
field (1955; 1961; 1964) as well as
numerous other authors who have dis-
cussed anatomical characters in their
descriptions of new genera and species.
The definitions of genera and, for that
matter, of families and subfamilies in
the superfamily are not precise. For
this reason, the generic placement of
some commensals has changed fre-
quently. Information on the anatomy of
those type-species, which are otherwise
known only conchologically, is greatly
needed in order to establish a more
sound taxonomic foundation.
In this review, each major group of
hosts is considered. Original sources
are included in the bibliography. The
following is an alphabetical list of the
erycinacean genera here discussed and
the sections in which they are men-
tioned.
Achasmea Echiuroidea
Aligena Annelida
Ceratobornia Annelida, Arthropoda
Cycladella Mollusca
Cycladoconcha Echinodermata
Devonia Echinodermata
Divariscintilla Arthropoda .
Entovalva Echinodermata
Ephippodonta Porifera, Coelenterata,
Arthropoda
Fronsella Sipunculoidea
Galeomma Coelenterata
Jousseaumiella Coelenterata, Sipunculoi-
dea
Kellia Porifera, Bryozoa, Mol-
lusca, Echinodermata,
Arthropoda
Lasaea Mollusca, Echinoder-
mata
Lepton Annelida, Echinoder-
mata, Arthropoda
Libratula Coelenterata
Marikellia Porifera, Mollusca
Montacuta Sipunculoidea, Bryozoa,
Echinodermata
Mylitta Echinodermata
Mysella Sipunculoidea, Annelida,
Mollusca, Echinodermata
Nipponomontacuta Coelenterata
Parabornia Arthropoda
Peregrinamor Arthropoda
Phlyctaenachlamys Arthropoda
Potidoma Sipunculoidea, Annelida
Pseudopythina Annelida, Arthropoda
Rochelfortia Sipunculoidea, Arthropoda
Scintillona Echinodermata
Scioberetia Echinodermata
Serridens Mollusca
Sphaerumbonella Coelenterata
Synapticola Echinodermata
Thyreopsis Coelenterata
Vasconiella Arthropoda
PORIFERA
Cotton and Godfrey (1938) recorded
Marikellia vincentensis 4 from the Gulf
of St. Vincent, Australia, in the hollows
of an unnamed sponge. Three species
of Ephippodonta, from Australia: E.
macdougalli Tate, E. lunata Tate, and
Е. turnbullae Buick and Bowden, live in
association with an unnamed, orange-
colored sponge at the opening of the
muddy burrows of the shrimp Axius
(Tate, 1889; Matthews, 1893; Buick and
Bowden, 1951).
COELENTERATA
From unnamed corals, Adams (1868)
described Thyreopsis coralliophila from
Mauritius and Pease (1865) named Li-
bratula plana from the Central Pacific.
These species have been cited by Franc
(1960) as members of the genus Galeom-
ma.
Yamamoto and Habe (1961) established
Nipponomontacuta actinariophila, which
was found on an unnamed sea anemone
off Honshu, Japan. Coen (1933) des-
cribed a new genus andspecies,Sphaer-
umbonella brunelli, as occurring in a
burrow, which was thought to be that
of an annelid, at the base of a mad-
reporarian coral at Massaua, Eritrea,
on the Red Sea.
Kuroda (1946) figured and described
Ephippodonta murakamii from Japan, and
2Dell (1964) included Marikellia Iredale in the
synonymy of Kellia Turton.
SYMBIOTIC ERYCINACEAN BIVALVES 185
Arakawa (1960) presented ecological data
which indicate that this species of Ephip-
pondonta, unlike the Australian species,
lives attached to the deep sea coral
Dendrophyllia cribosa Milne-Edwards
and Haime.
From the Ceylon coast in the Gulf
of Manaar, Bourne (1906) named 2 spe-
cies of the genus Jousseaumia, later
renamed Jousseaumiella (Bourne, 1907).
The 2 species, J. heteropsammiae and
J. heterocyathi, live in the burrows of
the sipunculid Aspidosiphon, in the corals
Heteropsammia michelini Milne-Ed-
wards and Haime and Heterocyathus
aequicostatus Milne-Edwards and
Haime, respectively. To one of these
species of Jousseaumiella, Bouvier
(1894; 1895) applied the name Kellia
deshayesii and Shipley (1903) referred
to them as unknown species of Mysella.
SIPUNCULOIDEA
Pelseneer (1928) listed some ex-
amples of the symbiotic relationships
between sipunculids and mollusks. Mon-
tacuta (Litigiella) glabra (Fischer),
which according to Pelseneer (1911)
is synonymous with Erycina сиепой
Lamy and Montacuta perezi Pelseneer,
has been found on Sipunculus nudus
Linnaeus at Arcachon, France (Pelsen-
eer, 1909; Franc, 1960). In Japan,
Fronsella ohshimai Habe may attach on
the skin near the anus of S. nudus
(Habe, 1964). Species associated with
Golfingia vulgare (de Blainville) on the
coast of France include Mysella bidentata
and Potidoma clarkiae (Clark) (Pelsen-
eer, 1925). Deroux (1961) placed Lep-
ton clarkiae in the genus Potidoma.
In England, M. bidentata and P. clarkiae
have been reported in association with
Phascolosoma pellucidum (Orton, 1923;
Winckworth, 1924a) and with P. elon-
gatum Keferstein (Gardiner, 1928; Sal-
isbury, 1932; Popham, 1940).
A more complex commensal relation
occurs among the species of Jousseau-
miella. Two species of this genus have
been recorded in association with the
corals Heteropsammia and Heterocy-
athus in the Gulf of Manaar by Bourne
(1906) where they live in the burrows
of Aspidosiphon, sometimes imbedded
in the skin of the posterior portions
of the sipunculid. From Indonesian
waters, Knudsen (1944) described Jous -
seaumiella concharum, a protandric her-
maphrodite with brood protection, which
attaches to the Mitra shell used by
species of Aspidosiphon or Phascolion.
In Europe, Phascolion strombi (Mon-
tagu) is the center of a complex etho-
logical relationship (Perez, 1924; 1925).
This sipunculid inhabits discarded shells
of gastropods including Nassarius, Mur-
ex, and Aporrhais. In the example given
by Perez, P. strombi lived in the shells
of Turritella communis Risso and Zi-
zyphinus |=Calliostoma] conuloides La-
marck. The bivalve Montacuta phas-
colionis Dautzenberg was attached atthe
orifice where the sipunculids generated
water currents. In addition, the small
ectoparasitic gastropodOdostomia (Auri-
stomia) perezi Dautzenberg, a syllid
polychaete, Langerhansia cornuta (Rath-
ke), and the endoproct bryozoan Loxo-
soma may also be in the association.
In the western Atlantic, Phascolion
strombi lives in the empty shells of
Nassarius trivittatus (Say) and Eupleura
caudata (Say). Hampson (1964) showed
that Rochefortia (Pythinella) cuneata
(Verrill and Bush) lives in association
with this sipunculid, much as Monta-
cuta phascolionis does in Europe.
ECHIUROIDEA
Habe (1962) described and figured
Achasmea thalassemicola, attached to
the body and proboscis of the echiu-
roid Thalassema mucosum Ikeda, from
the intertidal zone of Tomoe Bay, Tom-
ioka, Japan.
BRYOZOA
Madsen (1949) recorded an associa-
tion between Kellia rubra (Montagu)
and an unnamed bryozoan in Iceland.
186 K. J. BOSS
Perez (1924) showed that the endoproct
Loxosoma may be involved in the com-
plex commensal relationship between
Montacuta phascolionis and Phascolion
strombi.
ANNELIDA
Stimpson (1855) described Lepton
[Ceratobornia] longipes from South Car-
olina and noted that it lived in “holes
of marine worms and fossorial crus-
taceans.” Lepton squamosum (Montagu)
and an unnamed species of Kellia were
listed from annelid burrows by Fischer
(1887). The occurrence of Mysella
bidentata in the burrows of Nereis has
been reported by Winckworth (1923) and
Orton (1923). Anthony (1916) cited an
unnamed species of Montacuta in the
tubes of Eunereis longissima (Johnston)
at Boulogne. In the eastern Pacific,
Pseudopythina rugifera (Carpenter),
well-known as an ectoparasite of the
crustacean Upogebia, lives attached by
its byssus to the ventral surface of the
polychaete worm, or sea mouse, Aph-
rodite (Oldroyd, 1924; MacGinitie and
MacGinitie, 1949). For the European
species, Lepton subtrigonum Jeffreys,
Deroux (1961) established the genus
Potidoma, which also includes Lepton
clarkiae, a commensal of sipunculids.
Potidoma subtrigona attaches byssally
to the medial segments of the ventral
surface of the polychaete Polydontes
maxillosus (Ranzani). In Barnstable
Harbor, Massachusetts, Aligena elevata
Stimpson has been found attached to the
lower end of Clymenella torquata(Leidy)
(Sanders et al., 1962).
MOLLUSCA
AMPHINEURA. Kelsey (1902) found
Serridens oblonga (Carpenter) nestling
under the mantle or clinging to the
shell of /schnochiton conspicuus (Car-
penter) at Point Loma and Pacific Beach,
California. In adding [schnochiton mag-
dalenensis Hinds to the list of known
hosts for S. oblonga, Burch and Burch
(1944) confirmed the observations of
Kelsey and noted that the commensals
could also be found among the gills
and on the bottom of the foot of the
chitons. In their study on the fauna
of Monterey Bay, California, Smith
and Gordon (1948) recorded S. oblonga
on Ischnochiton heathiana (Berry).
GASTROPODA. Lasaea scalaris
Philippi has been found attached to
the aperture of Turricula teresiae Ten-
ison-Woods in South Australia by Verco
(1913), who suggested that a possible
commensal relationship existed between
the 2 species. Kellia rubra (Montagu)
has been found among the tubes of
Vermetus corallinaceus Tomlin at Oude-
krall, South Africa (Barnard, 1964).
Mysella bidentata (Montagu) has been
associated with Akera nana Jeffreys and
A. bullata Müller (Winckworth, 1923).
BIVALVIA. Members of the genus
Lasaea often nestle among the byssi
of mytilids (Keen, 1938). Haas (1942)
reported a specificity in these habits
within Г. cistula Keen and Г. subviri-
dis Dall. Both species preferably live
in the shell or within the byssal strands
of Brachidontes (Hormomya) multi-
formis Carpenter in California, and
are not found in the byssus of Mytilus
californianus Conrad. North of Point
Conception, at the end of the range
of B. multiformis, both species of Lasaea
occur in the byssus of М. californianus.
Haas also reported that in Peru, L.
miliaris Philippi lives in the byssus of
Brachidontes granulatus Hanley. A
Similar situation obtains among the spe-
cies of Marikellia [=Kellia] in Australia
where Laseron (1956) has reported that
certain species are found among the
byssus of the mussel Trichomya hir-
suta (Lamarck).
Carpenter (1865) recorded a number
of species, including those of his genus
Cycladella on the shells of Chama and
Spondylus. The species were nestlers
and no indication of commensal rela-
tionships was evident.
Packard (1918) found Kellza laperousii
Deshayes in pholadid borings in San
SYMBIOTIC ERYCINACEAN BIVALVES
Francisco Bay, and Pelseneer (1922)
found Mysella bidentata on Barnea can-
dida (Linnaeus) in Europe.
ECHINODERMATA
ECHINOIDEA. Many reports in the
literature document the occurrence of
Montacuta substriata (Montagu) and M.
ferruginosa (Montagu) with various echi-
noids. Jeffreys (1863) and Pelseneer
(1925) listed the species of echinoids
upon which M. substriata could be found.
Among them were: Spatangus purpureus
Miiller (=S. meridionalis Risso), Cidaris
cidaris (Linnaeus), Echinocardium fla-
vescens (Müller), Brissopsis lyrifera
(Forbes), and Echinus esculentus Lin-
naeus. M. substriata attaches itself
by 2 or 3 byssal threads to the oral
spines of S. purpureus. This behavior
has been reported from numerous Eur-
opean localities (Brusina, 1865; Norman,
1891a; Grieg, 1896; Madsen, 1949; Pop-
ham, 1940; Pelseneer, 1925; Deroux,
1961). Also, Vayssiére (1920) found
Lasaea rubra on Spatangus.
Certainly the most remarkable situa-
tion which involves the commensals
of S. purpureus is that reported by
Marshall (1891). When both Montacuta
substriata and M. ferruginosa live at-
tached to the urchin, the specimens of
M. substriata attach only to the spines
on the ventral region of the host where-
as individuals of M. ferruginosa are
on the dorsal spines. Outside the range
of M. substriata, M. ferruginosa is found
on both oral and aboral regions of its
host. This example is a fine illus-
tration of Gause’s law of competitive
exclusion.
As early as 1848, Lovén recorded the
occurrence of M. ferruginosa on Bris-
sopsis lyrifeva in Sweden, and Giard
(1886) found it on Echinocardium cor-
datum (Pennant) on the French coast.
Marshall (1891) noted M. ferruginosa
living in the burrow of E. cordatum at
Torbay, England, while in another popu-
lation he discovered the bivalves attached
to the spines of the urchin. The larger
187
or more adult specimens of M. ferrug-
inosa live opposite the anal siphon ofthe
urchin but younger individuals are at-
tached to the urchin’s oral spines (Allen
and Todd, 1900; Salisbury, 1932; Winck-
worth, 1924a; Moore, 1933; Popham,
1940; Deroux, 1961; Morton, 1962).
Similarly, at Port Philipp, Victoria, Aus-
tralia, Montacuta semiradiata Tate lives
on the spines oí Е. cordatum (Tate,
1889; Cotton and Godfrey, 1938; Franc,
1960). In Japan, Montacuta echinocardio-
phila has recently been described by
Habe (1964) as attaching to E. cordatum.
The Antarctic spatangoid, Abatus ca-
vernosus (Philippi), previously referred
to such genera as Spatangus, Tripylus,
and Hemiaster, is host to a number of
commensals. Dall (1876) described the
first of these asLepton parasiticumfrom
the ambulacra or the surface of the
test of an unnamed species of spa-
tangoid dredged in Royal Sound, Ker-
guelen Island. Smith (1877) substan-
tiated Dall’s discovery andindicated that
the host species is A. cavernosus, Later
Bernard (1896) described the curious
Scioberetia australis which lives com-
mensally in the brood pouches of A.
cavernosus, and then Grieg (1929) named
Montacuta christenseni, another com-
mensal bivalve living attached to the
Spines around the peristome on the
ventral side of the sea urchin. Morten-
sen (1936; 1951) mentioned an unnamed
Lepton, attaching in great numbers to
A. cavernosus and filling up the petals
and apical system of the urchin. Ac-
cording to him, this species is not the
L. parasiticum of Dall.
Soot-Ryen (1959) referred a species
of Lepton to parasiticum of Dall which
was found living on Tripylaster philip-
pi Gray in southern Chile. Dell (1964)
has indicated that the species found by
Soot-Ryen could not be the same as
L. parasiticum.
HOLOTHUROIDEA. Semper (1868)
made early mention of the occurrence
of ectocommensal bivalves on synaptids
when he recorded but did not describe
a small pelecypod living on Protankyra
188
similis (Semper) in the Philippines.
The first documented case of “para-
sitism” of bivalves in holothurians was
presented by Voeltzkow (1890) who named
and described Entovalva mirabilis, a
species living in the oesophagus of
Synapta [Leptos ynapta] ooplax von Mar-
enzeller 3. Schepman and Nierstrasz
(1913) added to the original description
and gave ecological data on E. mira-
bilis.
Entovalva (Devonia) perrieri was des-
cribed by Malard (1903), who found the
ectoparasite on the posterior portions
of the body of the synaptid Leptosyn-
apta inhaerens (Müller) at Saint-Vaast-
la-Hougue, France. He erected the genus
Synapticola for the species but since
this name was preoccupied in the Crus-
tacea, Winckworth (1930) proposed De-
vonia. Anthony (1916) studied the mor-
phology of E. perrieri in detail, noted
its relationship to Е. mirabilis, and
considered the species a member of
Entovalva. He found that the small
bivalve was usually attached to the pos-
terior portions of the body of the syn-
aptid but occasionally was found at the
base of the tentacles of its host. He
also indicated that the glochidial-type
larval form found by Herpin (1915)
at Cherbourg may be a stage in the
life history of Е. perrieri. Clench
and Aguayo (1931) recorded E. perrieri
at Woods Hole, Massachusetts, on Z.
inhaerens and thus extended the known
range of the ectoparasite to the western
Atlantic. In England, Popham (1940)
discussed some aspects of the mor-
phology of the mollusk and noted that
it attached to and progressed over the
surface of the holothurian by means of
its foot.
Another species of Entovalva, E. sem-
peri Ohshima, occurs in the Pacific
Ocean and was reported by Ohshima
3Spärck (1931) has indicated that the holothur-
ian in which E. mirabilis lives is Patinapta
crosslandi (Heding) not Synapta ooplax von
Marenzeller.
K. J. BOSS
(1929; 1930; 1931) from Kyushu, Japan.
This species infests 2 apodous holo-
thurians, Leptosynapta inhaerens, the
usual host for Entovalva, and Protankyra
bidentata (Woodward and Barrett). From
Isigaki Island in the Ryukyu Islands,
Kawahara (1942) found another Devonia,
E. (D.) ohshimai attached to the body
wall of Leptosynapta ooplax (von Mar-
enzeller).
A fifth species of Entovalva, E. major,
was described by Bruun (1938) from the
Biological Station at Ghardaga, Egypt,
on the Red Sea. This species was
associated with the aspidochiroten Mer-
tensiothuria fuscocineria (Jaeger)
|=Holothuria curiosa (Ludwig)]. On the
basis of circumstantial evidence, Bruun
suggested that E. major probably lives
in the cloaca of the holothurian.
Spirck (1931) established the new
genus and species, Cycladoconcha am-
boinensis, from Indonesian waters,
where it lives in small pouches in
the oesophagus of the apodous holothurian
Patinapta laevis (Bedford). This pe-
culiar endoparasitic relationship is very
similar to that of Entovalva mirabilis
in the oesophagus of Patinapta cross-
landi mentioned previously. Cyclado-
concha is closely related to Entovalva.
Montacuta donacina (Wood) and M.
percompressa Dall have been found on
Leptosynapta inhaerens (Bateson, 1923;
Gray, 1933; М. donacina has also been
found on Labidoplax digitata (Montagu)
(Franc, 1960).
Morton (1957) discussed the mor-
phology and parasitic habits of Scintil-
lona zelandica (Odhner) on the synaptid
Trochodota dendyi Mortensen, in New
Zealand.
OPHIUROIDEA. At Salcombe, Eng-
land, Mysella bidentata (Montagu) lives
in association with the brittle stars
Ophiocnida brachiata (Montagu) andAm-
Рита filiformis (Müller) (Winckworth,
1923). At Plymouth, Orton (1923) found
M. bidentata in the vicinity of the disc
of O. brachiata and reported a third
organism in this commensalistic asso-
ciation, namely, the polynoid polychaete
SYMBIOTIC ERYCINACEAN BIVALVES 189
Harmothoé lunulata (delle Chiaje). Pop-
ham (1940), in her study of the mantle
cavity of the Erycinacea, noted that
M. bidentata does not attach itself to
its ophiuroid host.
ARTHROPODA
DECAPODA. Living along the muddy
burrows of the shrimp Axzus plecto-
rhychus (Strahl), are the 3 Australian
species of Ephippodonta: E. macdougalli
Tate, E. lunata Tate, and Е. turnbullae
Buick and Bowden (Tate, 1889; Buick and
Bowden, 1951). A sponge may also live
along with these species in the burrow.
In addition to the species of Ephip-
podonta, 3 species of Mylitta: М. tas-
manica Tenison-Woods, М. gemmata
Tate, M. deshayesiana d’Orbigny, as well
as an unnamed species of Kellia, may
also be found in the burrows of Axzus
(Matthews, 1893; Cotton and Godfrey,
1938). The morphology of Ephippodonta
has been discussed by Woodward
(1893).
In England, Lepton squamosum (Mon-
tagu) lives in the burrows of Upogebia
deltaura (Leach) and U. stellata (Mon-
tagu) (Norman, 1891а; Winckworth, 1924
a and b; Salisbury, 1932), and in France,
Lepton nitidum Turton has been found
attached by its byssus to U. deltaura
(Pelseneer, 1925).
One of the best known cases of a
bivalve attached to a crustacean is that
of Pseudopythina rugifera (Carpenter)
which affixes by means of it byssus to
the ventral portions of the abdominal
segments of the blue mud shrimp of
western North America, Upogebia puget-
tensis (Dana). Stimpson (1857) first noted
this relationship; it was subsequently
reported by, among others, Norman
(1891b), Harrington and Griffin (1898)
and Dall (1899), who pictured the at-
tached bivalve. The Lepton rude des-
cribed by Whiteaves (1880) is synony-
mous with P. rugifera. MacGinitie and
MacGinitie (1949) reported that P;
rugifera may also be encountered
on the venter of the sea mouse Aph-
rodite even more often than on the mud
shrimp. From Japan, Shöji (1938) des-
cribed Peregrinamor ohshimai,a gale-
ommatid commensal, which attaches by
its byssus tothe ventral portion and along
the median line of the cephalothorax of
the burrowing shrimp Upogebia major (de
Haan).
Stimpson (1855) discovered Lepton
longipes, which he noted living in the
“holes of marine worms and fossorial
crustaceans” in South Carolina. Nor-
man (1891a) identified some of the hosts
of Г. longipes as Callianassa major
Say and Upogebia affinis (Say). Dall
(1899) placed Г. longipes in the genus
Ceratobornia. Oldroyd (1924) added
that both Pseudopythina compressa Dall
and P. myaciformis Dall were also com-
mensal with crustaceans. Rochefortia
pedroana Dall attaches to the hairs of
the legs and the ventral regions among
the gills of the large sand crab, Ble-
pharipoda occidentalis Randall in Cal-
ifornia (Burch and Burch, 1944; Emer-
son, 1944). Incidentally, the nonerycina-
cean bivalves Mytilus edulis Linnaeus
and Cerastoderma edule (Linnaeus) have
been found attached to the abdomen of
Carcinides maenas (Linnaeus) (Fischer,
1930; Wolff, 1959).
STOMATOPODA. Kuroda (1937) illus-
trated Pseudopythina subsinuata (Lis-
chke) attached by its byssus to the first
abdominal segment of Squilla oratoria
de Haan from Japan. From the area
of the Great Barrier Reef in Australia,
Popham (1939) described Phlyctaena-
chlamys lysiosquillina which lives com-
mensally in the burrows of Lysiosquilla
maculata (Fabricius). Powell (in Mor-
ton, 1957) suggested that Divariscintilla
maoria Powell of New Zealand, which
is conchologically similar to Vasconiella
of the eastern Atlantic (Kisch, 1958),
may live attached to a species of Ly-
siosquilla. Moore (1961) noted the pre-
sence of a small bivalve, which he ten-
tatively referred to as Lepion, on Ly-
siosquilla scabricauda (Lamarck) in
Mississippi; Boss (1965) has described
this species as Parabornia squillina
190 K. J. BOSS
found attached to the ventral surface
of the abdomen and thorax of L. sca-
bricauda from the Caribbean coast of
Panama.
CONCLUSION
Some general principles may be stated
from even a casual analysis of the ex-
tensive list of individual commensals
and their hosts. The hosts are ex-
clusively invertebrates, and certain
groups of invertebrates are preferred.
Two common ecological or behavioral
factors may be responsible for these
associations. Most of the hosts are
slow moving, almost sessile forms,
which burrow in sandy or muddy bottoms,
and further, most of them obtain their
food by filter feeding. The relative
immobility of the hosts facilitates sim-
ple attachment or association by the
commensal and the currents created by
the processes of filter feeding generate
a favorable environment for the small
mollusks, which are themselves filter
feeders. Natant or more mobile hosts,
such as the higher crustaceans, carry
the small bivalves attached ventrally in
a relatively protected position. The re-
lationships between erycinacean bivalves
and their hosts appear to be predomi-
nantly commensalistic, and no evidence
exists of deleterious or pathologic ef-
fects on the hosts, even when the mol-
lusks live inside the host or attach
directly to its epidermis. In assuming
a commensalistic existence, the erycina-
ceans have evolved toward highly
specialized habits with concomitant mor-
phological adaptations, including the en-
closure of the shell by the mantle and
the reduction of the shell.
ACKNOWLEDGMENTS
R. B. Manning, D. L. Pawson, and
M. E. Jones, of the U. S. National
Museum read and criticized the manu-
script in regard to their specialized
areas of study. J. Rosewater, Division
of Mollusks, U. S. National Museum,
R. Robertson, Department of Mollusks,
Academy of Natural Sciences, Phila-
delphia, A. H. Clarke, National Museum
of Canada, Ottawa, B. Collette, Ichthyo-
logical Laboratory, Burean of Commer-
cial Fisheries, Washington, D. C., and
A. S. Merrill, Bureau of Commercial
Fisheries, Oxford, Maryland, offered
suggestions and criticisms.
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lives attached to the external surface of
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SYMBIOTIC ERYCINACEAN BIVALVES
RESUMEN
BIVALVOS ERYNACEOS SIMBIOTICOS
Este trabajo sumariza la ocurrencia de comportamiento simbiötico entre repre-
sentantes de los eulamelibranquios de la superfamilia Erycinacea. Casos indivi-
duales de comensalismo, mutualismo, o hasta ectoparasitismo y tambien aparente
endoparasitismo, se presentan documentados. Los moluscos se discuten en relacion
a sus huéspedes con breves anotaciones concernientes a la causa general de esas
asociaciones.
195
MALACOLOGIA, 1965, 3(2): 197-210
ECOLOGY OF CYRTODARIA SILIQUA AND HISTORY OF THE
GENUS CYRTODARIA (BIVALVIA: HIATELLIDAE)
K. N. Nesis
Polar Research Institute of Marine
Fisheries and Oceanography (PINRO)
Murmansk, USSR
ABSTRACT
Cyrtodaria siliqua (Spengler) is distributed from the northern extremity of the
Great Newfoundland Bank to the Georges Bank; it inhabits fine sand bottoms
down to 500m, but mainly at depths of 50-150m, and is found below 250m only in
the areas of intensive downward movements of water; it was observed at tem-
peratures of -1.0 to +5. 7°C and at salinities of 32.3 to 34. 2° /00.
The species is a mobile suspension feeder of incoherent bottoms. Its require-
ments of depth and substrate are connected with its type of feeding. It probably
cannot breed at constant low temperatures, for which reason it does not pene-
trate north of the Great Newfoundland Bank. In its range C. siliqua is a West-
Atlantic north-boreal species, and in its thermal requirements a low-arctic-
boreal one.
The genus Cyrtodaria Daudin is of Atlantic origin. It was formed during the
transition of the Paleogene to the Neogene, its ancestors possibly living in the
seas of the South-Russian geosyncline during the Paleogene; by the end of the
Neogene it spread to the shoals of the North Atlantic and the Arctic and broke up
into a number of closely related species. Due to the pleistocene glaciations these
‚ species died out off the shores of Europe, and the West-Atlantic С. siliqua was
driven to the south. In the period of the postglacial climatic optimum it spread
as far as northwestern Greenland, but due to the increased depth of the Denmark
Strait it could not again penetrate to Iceland where it hadlived in preglacial times
(Nesis, 1961).
C. kurriana, the second living species of the genus, is a circumpolar high-
arctic species inhabiting only brackish waters of the coastal shallows; it origi-
nated in the Arctic at the beginning of the Pleistocene. Its ancestors were rela-
tively warmth-loving and lived at normal sea water salinities. Due to the re-
peated drying of the shelves in the periods of eustatic regressions, it was driven
into the brackish water areas. At the beginning of the postglacial, or in one of
the interglacials, it migrated southward as far as the Amur estuary, but during
subsequent warming and rise in salinity of the coastal waters of the Far Eastern
Seas it died out in the intervening areas. The present warming of the Barents
Sea may also lead to a further decrease in the range of this species.
The genus Cyrtodaria demonstrates the 2 main trends of species formation;
the “linear or chain” and “bouquet” types of E. F. Gurjanova (1951). The evo-
lution of Cyrtodaria according to the “linear” type resulted in the transformation
of ancestors requiring higher temperatures (a comparatively rare example of
high-arctic species of Atlantic origin) into the Artic species C. kurriana, each
species of the chain retaining the morphophysiological adaptations toa definite
type of feeding.
INTRODUCTION tioned very rarely in scientific litera-
ture and are familiar only to taxono-
Cyrtodaria Daudin, 1799 is one of the mists. The genus consists of only 2
little-studied genera which are men- living species: С. siliqua (Spengler,
(197)
198 К. N. МЕБ
1793)1 and С. kurriana Dunker, 1862
which for a long time were united
erroneously (Dautzenberg and Fischer,
1912; Lamy, 1925). We have some
data, though very limited, on the ecology
of C. kurriana, but little was known of
С. siliqua, whose distribution even was
not quite clear, although the species is
known since the 18th century. This lack
of information is especially strange
because this species is one of the most
frequent bottom organisms on the Great
Newfoundland Bank andthe favourite food
of cod 2 haddock 3 yellowtail American
dab® and other fishes. The frequency of
Cyrtodaria in the food of cod sometimes
reaches 20% (by weight even more).
Taking into account that millions of
people indifferent countries from Canada
to Africa and from England to Brazil
have been eating Newfoundland cod for
aimost 6 centuries, we can say that to
a certain extent, people have been eating
transformed Cyrtodaria. It is the
abundance of benthos there that provides
the great abundance of cod and haddock
on the Newfoundland Banks which has
attracted fishermen into this area as
far back as Pre-Columbian times.
The present data on the distribution
and ecology of C. siliqua were obtained
from the study of the collections made
by PINRO expeditions in the period
1954-1960, from 2 research vessels:
the “Sevastopol” (Cruise I, inApril-May
1954, collection by A. D. Starostin;
Cruise 14, in July-August 1959, col-
lection by the author; Cruise 16, in
March-April 1960, collection by K. P.
Yanulov, A. A. Georgiev and others;
Cruise 17, in July-August 1960, col-
lection by the author) and the “Odessa”
(Cruise 1, in March-April 1958, col-
INorthern propeller clam, or banks clam.
2Gadus morhua L.
3Melanogrammus aeglefinus (L.).
4Limanda ferruginea (Storer).
9 Hippoglossoides platessoides (Fabricius).
lection by Mrs. I. N. Sidorenko). The
collections were gatheredby commercial
trawl, by the Sigsbee trawl and the
bottom grab “Ocean 50”. Investigations
were carried out in the northwestern
Atlantic, on the shallow water banks of
the outer shelf and the upper bathyal
waters of a rather extensive area from
the northern extremity of Labrador to
the central part of Nova Scotia. С. sili-
qua was encountered at more than 70
stations (Fig. 1).
According to the data available in the
literature (Packard, 1867; Gould, 1870;
Verrill, 1880; Whiteaves, 1901), this
species is to be found throughout the
shallow water area of the Gulf of St.
Lawrence right up to the Strait of Belle
Isle, on the Newfoundland Banks, off
Nova Scotia, in the Gulf of Maine and
on the Georges Bank. The southern
boundary of its range runs south-west
of Cape Cod. It is worth noting that we
never found С. siliqua on the outer shelf
north of the Great Newfoundland Bank.
Neither was it encountered on the
Flemish Cap Bank where we collected
more than 100 samples. Judging from
its area of distribution, С. siliqua is a
West Atlantic north-boreal species.
Cyrtodaria siliqua
The outward appearance of this mol-
lusk is rather peculiar. It can reacha
rather big size; up to 8-10cmin length.
The shell sits on the body of the mol-
lusk like a tight coat on a fat man,
gaping in front, from below and from
behind and the valves closing only near
the beak. The mantle lobes are grown
together almost throughout the whole
body length, leaving an opening for the
foot only in front, and are also grown
tightly to the shell. On the ventral
side of the body that portion of the man-
tle which is free from the shell, is
especially fat and fleshy. The entirely
united siphons are also rather fleshy.
The internal structure of the mollusk is
typical of Hiatellidae (Woodward, 1875).
The banks clam, Cyrtodaria siliqua,
completely buries itself into the ground
ECOLOGY OF CYRTODARIA 199
70 65 60 55 ‚50 45
50
45
FIG. 1. Distribution of Cyrtodaria siliqua on the outer shelf and shallow banks off Newfoundland
and Nova Scotia as revealedby the PINRO expeditions in the period, 1954-1960 (depth in fathoms).
1. Great Newfoundland Bank, 2. Flemish Cap Bank, 3. Banquereau Bank, 4. Gulf of St. Law-
rence, 5. Georges Bank.
200 K. N. NESIS
(Brunel, 1960), but not very deeply:
the depth can hardly exceed a few cm
as its siphons cannot extend greatly, in
view of the small size of the pallial
sinus, and since the foot is small and
weak. It is quite clear that this mollusk
can easily become a prey of various
fishes. Fishes usually swallow the
whole of the mollusk, but sometimes cod
bites off only the siphons and the ven-
tral part. On the Great Newfoundland
Bank this clam is more common in the
food of cod than any other mollusk,
probably because cod cannot take clams
which bury themselves very deeply into
the ground; further, cod evidently avoid
preying upon organisms whose body is
completely covered by the shell. Had-
dock also readily eat banks clams (Ho-
mans and Needler, 1946).
The whole structure of С. siliqua
shows that this organism is a typical
filter feeder of the near-bottom water
layer. According to A. I. Savilov’s
classification (1961), it must be placed
with the mobile suspension feeders of the
incoherent bottoms. The requirements
of this mollusk regarding depth and type
of bottom are closely connected with its
manner of feeding, С. siliqua is common
at depths down to 500m: from 51-472m
(Verill, 1885), 9-90m (Johnson, 1934),
4-165m (Bousfield, 1960), 38-500m (our
observations); but it obviously prefers
the depths of 50-150m, at which depths
2/3 of all our collections were taken.
This organism is rarely found at less
than 50m (Fig. 2). Our data reveal
that 125 m is the average depth of its
distribution. The species shows marked
restriction to certain depths: the stan-
dard ratio of factorial and random de-
viates calculated by the one-factor com-
plex corresponds to a probability ex-
ceeding 0.999. Of the various factors
conditioning the distribution of the spe-
cies, depth is assigned 40% of the total
influence. In fact, the influence of depth
is even more pronounced, since below
250 m C. siliqua was found only on the
eastern slope of the Great Newfoundland
Bank, in the area of the intensive des-
%
50
0 50 100 150 200 250 300 350 400 450 500
FIG. 2. Bathymetrical distribution of Cyrto-
daria siliqua (depth in meters).
cending movements of waters. There, at
250-500 m, there prevail the conditions
characteristic of shallow waters.
С. siliqua lives mainly in fine sand,
avoiding the coarse-sand bottoms in the
shallowest parts of the banks.
The distribution of С. szliqua in the
Northwest Atlantic, both horizontal and
vertical, coincides almost entirely with
that of the sand dollar Echinarachnius
parma Lamarck (Nesis, 1962), which is
extremely abundant in that area. This
sea urchin is also a suspension feeder
of the near-bottom water layer (Sokolova
and Kuznetsov, 1960). The zone where
mobile suspension feeders of the inco-
herent bottoms live is limited by the
upper and middle parts of the broad
platform shelves (Neiman, 1961) with
fine-sand bottoms and considerable de-
position of suspended matter. Above
and below this zone the quantity of sus-
pended matter in the near-bottomlayers
decreases: in the zone of development of
the coastal epifauna the particles of
detritus are suspended by reason of the
intensive water movements and are car-
ried above the bottom; on the other hand,
the lower sublittoral and bathyal areas
are located farther from the shore, which
is the main source of food materials
for the benthos. С. siliqua avoids the
shallowest depths because of the de-
crease in the amount of food available
for buried mollusks and because of hard
bottoms which are unfavourable for them.
In the Newfoundland area the Atlantic
waters wash the continental slope, while
ECOLOGY OF CYRTODARIA 201
the shallows are covered with arcticand
local water masses of lower salinity
and sharp seasonal and year-to-year
temperature fluctuations (Schott, 1942;
Elizarov, 1961). Evidently, the banks
clam, an inhabitant of shallow water
areas, can withstand considerable de-
crease in temperature and salinity. We
found Cyrtodaria at temperatures from
-1.0°C to 5.7°C (+1.15°C on the average)
and salinities from 32.30/00 to 34.29/00
(33.29/00 on the average). The fact that
С. siliqua occurs more frequently in
shallow waters explains why it is absent
from the Flemish Cap Bank: the
waters of the cold Labrador Current
do not approach the bank, and the strait
separating the Flemish Cap Bank from
the Great Newfoundland Bank is too deep
(1200 m) for Cyrtodaria to cross it.
Why does С. siliqua not occur to the
north of the Great Newfoundland Bank?
Presumably this absence is connected
with the reproductive postulates of this
species, since it is well known that re-
production and the early stages of de-
velopment are the most “vulnerable”
periods in the life cycle of aquatic organ-
isms. The reproductive habits of the
banks clam are unknown, therefore we
can only draw an analogy with the before-
mentioned Echinarachnius parma. The
northern part of the Great Newfoundland
Bank is the boundary of the boreal zone,
the limit of distribution of a number of
boreal and north-boreal species and of
one of the most important north-boreal
communities, the Echinarachnius parma
community. The causes of this pheno-
menon are more fully discussed in an-
other article (Nesis, 1962). Here, it is
merely pointed out that, in our opinion,
the distribution of these animals to the
north is restricted by the narrow tem-
perature range within which they can
reproduce.
Adult specimens of north-boreal spe-
cies are usually highly eurythermic,
but cannot breed at temperatures below
a certain limit, particularly at negative
temperatures (Runnström, 1927; Thor-
son, 1952). The short duration of the
period of mass development of phyto-
plankton in the Labrador waters is of
great importance for species with plank-
tonotrophic larvae.
As a rule, boreal species of animals
are not found at temperatures below
1-30 C (Blacker, 1957), but the banks
clam can withstand negative tempera-
tures as well. From its limits of
tolerance it is therefore to be regarded
as a low-arctic-boreal species.
Thus, it can be concluded that feeding
type and reaction to temperature during
the reproductive period are the main
factors influencing the distribution of
С. siliqua.
Cyrtodaria kurriana
The second species ofthe genus differs
from С. siliqua by a number of charac-
teristics such as shape, proportions,
colour of the shell, and especially by its
small size, usually up to 2 cm, some-
times 3-4 cm long. This circumpolar
high-arctic species inhabits only the
diluted coastal shallow waters (though
it never entered the fresh waters).
It is scarcely found below 50 m, its
usual depth being 10-20 m. Valves
of dead mollusks are, however, carried
with ice down to even the abyssal depths
of 2-3 km. С. kurriana is common
(Fig. 3) off the coasts of West and East
Greenland, Jan-Mayen, Spitsbergen,
Franz Joseph Land, Novaya Zemlya
(chiefly off the eastern coast), in the
south-eastern part of the Barents Sea
(Petchora estuary), in the Kara and
Laptev Seas, East Siberian Sea, where
it is especially abundant, off Wrangel
Island, along the northern shore of the
Chukchi Peninsula, in the Anadyr es-
tuary, in the weakly diluted part of the
Amur estuary (single findings), in the
Norton Sound, on the northern shores
of America east of Point Barrow, in
Baffin Bay, Hudson Bay, Hudson Strait,
and Ungava Bay (Derjugin, 1925; Mess-
jatzev, 1931; Gorbunov, 1946, 1952;
Uschakov, 1953; Filatova, 1957; Dall,
1919; Madsen, 1949; Thorson, 1951; La
Rocque, 1953; Ockelmann, 1958; Hiilse-
К. N. NESIS
202
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ECOLOGY OF CYRTODARIA 203
mann, 1962). The feeding habits of
this species are similar to those of
С. siliqua, but С. kurriana belongs to
the high-arctic communities of the con-
tinental runoff area where bivalve mol-
lusks prevail, i.e. the Portlandia aes-
tuariorum community in the Kara Sea
(Filatova and Zenkevitch, 1957) and the
Gomphina (Liocyma) fluctuosa com-
munity off East Greenland(Ockelmann,
1958).
History of the genus Cyrtodaria
Five fossil species of this genus have
been described. However, the oldest
of them, C. transcaspica Korobkov and
Mironova, 1955, from the Paleogene
(upper Eocene-lower Oligocene) of the
Transcaspian area (Mangyshlak, Ustj-
Urt, northern part of the Aral region,
Turgai, probably Fergana Valley), so
strongly differs, judging by its des-
cription (Iljina, 1955), from all other
representatives of Cyrtodaria by the al-
most central position of its beaks and
the absence of a pallial sinus, that it
cannot belong to the genus Cyrtodaria.
‚ The other 4 species are recorded in
the Neogene -Anthropogene® ofthe North-
Atlantic basin and the Arctic (Fig. 3):
C. neuvillei (Cossmann and Peyrot, 1909)
from the lower Miocene (Burdigalian)
in the vicinity of Bordeaux (Cossmann
and Peyrot, 1909); C. angusta (Nyst and
Westendorp, 1843) = C. vagina (Wood,
1857) from the middle Miocene-Pleis-
tocene of eastern England, the Nether-
lands and Belgium” (Wood, 1857; Cogels,
1874; Bell, 1918; Glibert, 1958); C.
camdenensis Dall, 1920, from the Plio-
cene of northern Alaska (Dall, 1920);
C. jenisseae Sachs, 1953, from the Ple-
istocene (chiefly early-and middle-Qua-
ternary sediments) of the Soviet Arctic,
from the Kolgujew Island to the Kha-
tanga River (Sachs, 1953; Strelkovetal.,
6
Anthropogene =the Quaternary Period.
A
A. I. Korobkov also mentioned this species
from the middle Oligocene of the Transcas-
pian area.
1959). Both recent species of Cyrto-
caria are found only in the Plio-Pleis-
tocene. As V. N. Sachs (1953) points
out, C. jenisseae is intermediate in
shell form between C. angusta and C.
siliqua. Judging by the pictures, these
3 species are rather closely related to
each other and are very near in their
form to C. neuvillei, whereas C. cam-
denensis more resembles C. kurriana.
Both the general paleoclimatic data
and the zoogeographical characteristics
of the other mollusks found in associa-
tion with the forms of Cyrtodaria ex-
amined give a rough idea of the thermal
tolerances of these fossil forms. Only
one recent form has been found together
with C. neuvillei: it is the world-wide
Hiatella arctica (s.l.) (Cossmann and
Peyrot, 1909). Paleoclimatic data in-
dicate that the climate of the Lower
Miocene in the vicinity of Bordeaux was
subtropical (Termier, 1952; Schwarz-
bach, 1950). In eastern England C.
angusta occurs more frequently in the
sediments of the Coralline Crag and in
the layers immediately underlying these
sediments. At that time the climate
was a little bit warmer than now (south-
boreal). The latest records of C.
angusta belong to layers which corres-
pond to the boreal climate (Reid, 1890).
In Belgium C. angusta has been found
together with boreal mollusks which are
now living in the North Sea and the Eng-
lish Channel (Glibert, 1958). Evidently,
this species was typically boreal, i.e.
lived in south-boreal as well as north-
boreal waters. Together with C. cam-
denensis other molluscan forms were
found which are very nearly related to
the recent arctic-boreal species Yol-
diella frigida (Torell), Natica clausa
(Broderip and Sowerby), Amauropsis
islandica (Gmelin) and also represen-
tatives of the genera Caecum, Cadulus
and Dentalium (Dall, 1920). Now these
3 genera are completely absent from
the Arctic, but are to be found in the
northernmost parts of the boreal zone.
Apparently, C. camdenensis was a north-
boreal or low-arctic boreal species.
204 K. N. NESIS
According to V. N. Sachs (1953),
C. jenisseae is a sub-arctic species,
i.e. according to our terminology, a
low-arctic-boreal Species.
The fossil specimens of C. siliqua
have been found in northern Iceland,
eastern Canada, and in northwestern
Greenland. In northern Iceland the old-
est layers with C. siliqua (Upper Plio-
cene or’ Eopleistocene® ) were formed
under climatic conditions which appar-
ently corresponded to the present cli-
mate of the English coasts, and the
youngest layers with C. siliqua (Lower
Pleistocene) under the climate prevailing
now off western Iceland. Whenthe water
temperature off the shores of northern
Iceland dropped to the present level
(now arctic species greatly predominate
there), С. siliqua disappeared (Bärdar-
son, 1925). In eastern Canada it has
been found in the postglacial sediments
of the area where it now lives (Packard,
1867; Richards, 1962). C. siliqua in-
habited the area off the shores of Green-
land only during the period of the post-
glacial climatic optimum (Laursen, 1944,
1950) when the water temperature was
about 2°C above that observed now, a
fact which, incidentally, confirms the
idea that the distribution of С. siliqua
in the northern direction is limited by
the water temperature.
С. kurriana is recorded in Pleistocene
and Holocene sediments in the Soviet
Arctic from the Polar Urals to the
Chukchi Peninsula and in Alaska under
conditions roughly similar tothe present
(Merklin et al., 1962; Merklin et al.,
1964; Principles of Paleontology, 1960;
Dall, 1919; Sachs, 1953; Strelkov et al.,
1959).
The above information enables us to
draw the following conclusions con-
cerning the history of the genus Cyrto-
daria. Having originated in the eastern
Atlantic some time during the transi-
tion between the Paleogene and the Neo-
8
Eopleistocene =the early Pleistocene until
the Mindel glaciation.
gene, from ancestors which, in the
Paleogene, inhabited the seas of the
South-Russian geosyncline,—derivatives
of the old Tethys—the genus Cyrtodaria,
by the end of the Neogene, had widely
spread in the shallow water areas or
the North Atlantic and the Arctic, which
was warm at that time, where it broke
up into a number of closely related
Species. The existence of a chain of
shallow-water shoals between Norway
and Greenland during the late Pliocene
promoted the penetration of Cyrtodaria
into the Northwest Atlantic (Nesis, 1961).
The species of Cyrtodaria required
relatively warm temperatures, being
boreal or low-arctic boreal, lived at the
normal salinity of sea water andreached
a size of 8-10 cm. During the Ple-
istocene glaciations they gradually died
out in the Arctic and East Atlantic,
while West Atlantic С. siliqua retreated
somewhere to the south, to the shores
of New England. During the postglacial
period С. siliqua rapidly spread to the
north and at the period of climatic
optimum it appeared off the coasts of
Greenland. After the end of the warmer
period it moved back to Newfoundland.
It could not reach Iceland again as it
now had to overcome the increased depth
of the Denmark Strait and the strong
contrary East-Greenland current. С.
siliqua has not been found in the post-
glacial deposits of Iceland (Bardarson,
1911; Pjetursson and Jensen, 1905).
C. kurriana, which is probably the off-
shoot of C. camdenensis, formed in the
Arctic at the beginning of the Pleisto-
cene period. The ecology of this spe-
cies is to a considerable extent asso-
ciated with the repeated drying of shelves
as a result of the Pleistocene eustatic
regressions. In the periods of regres-
sions the marine fauna could survive
in 2 situations only: either at great
depths, in bathyal and abyssal waters,
or in the brackish and fresh waters
(Zenkevitch, 1933; Gurjanova, 1939). The
descent of a shallow-water filter feeder
down to great depths being apparently
not possible, C. kurriana adapted to low
ECOLOGY OF CYRTODARIA 205
temperatures and salinities. An in-
herent eurythermy andeuryhalinity inits
ancestors must have made this adapta-
tion somewhat easier. It is possible
that the small size of this species, un-
usual for the genus in question, can be
explained by the influence of Arctic
conditions of existence or of freshening,
as the decrease in size of animals of
marine origin in the brackish waters is
well known (Zenkevitch, 1963).
Not so very long ago the distribution
of this species was evidently wider than
it is now. It is possible that 8,000-
10,000 years ago, at the very beginning
of the postglacial period when the Bering
Strait was formed, but when the coastal
waters were still very cold and diluted,
C. kurriana together with Portlandia
aestuariorum penetrated into the Pacific
Ocean and spread to the south down to
the Amur estuary, where these species
have been recorded by P. V. Uschakov
(1953; P. aestuariorum is doubtful).
This penetration might also have oc-
curred at the beginning of one of the
interglacial transgressions. With the
increase of salinity and rise in the
‘temperature of coastal waters C. kur-
riana perished and could survive only
in such places as the Amur and Anadyr
estuaries.
The area of C. kurriana distribution
in the Barents Sea is probably decreasing
due to the present warming. I. I. Mess-
jatzev (1931) found living specimens of
this species which, inhis opinion, is dying
out in the Barents Sea, onlyinthe coldest
parts of the western shore of Novaya
Zemlya: in the Zabludyashchaya and
Krestovaya inlets (north-west of the
Northern and south of the Southern
Islands). He found empty valves also
in the warmer areas of Novaya Zemlya
(Mityushikha and Belush’ya inlets), inthe
Kanin and Petchora regions of the Sea.
The collections at the Zoological Insti-
tute of the Academy of Sciences of the
USSR contain rather fresh valves of this
Species from the Teriberskaya inlet on
the Murman coast (collection of S. M.
Herzenstein, 1887), but now it is not
observed in this area (Uschakov, 1948;
Miloslavskaya, 1954). During our in-
vestigations in the southern and eastern
parts of the Barents Sea we also did
not observe С. kurriana beyond the limits
of the Petchora estuary, where it was
first recorded by K. M. Derjugin (1925)
and is abundant up to now.
What is the general conclusion from the
foregoing history of the genus Cyrto-
daria? First of all, C. kurrianais one of
the rather rare Arctic species of Atlantic
origin. Analysis of the paleontological
data confirmed the supposition of G. P.
Gorbunov (1952) about the Atlantic origin
of C. kurriana, which he made from the
study of its distribution area. Secondly,
we can see that, in the process of evolu-
tion of the genus, there occurred a
gradual adaptation of individual species
to the low temperatures: from sub-
tropical through boreal and low-
arctic-boreal to arctic conditions.
This adaptation was simultaneous with
the general cooling of the seas in the
Northern Hemisphere during the Neo-
gene-Anthropogene(Schwarzbach, 1950).
This type of species formation is very
near to the “linear, or chain type of
Species formation” proposed by E. F.
Gurjanova (1951). At the same time the
morphophysiological adaptation of spe-
cies to a certain feeding type remained
unchanged in all the species of Cyrto-
daria entering the chain and consequently
they were still restricted to shallow
water grounds.
When the ancestral form of Cyrto-
daria broke up into several closely re-
lated species during its initial spread
in the Atlantic and Arctic, the main
ecological peculiarities were retained.
This latter type of species formation
can be compared with the “bouquet”
type usually observed when animals first
appear in new areas. Thus, 2 main ways
of species evolution can be observed in
this small genus.
ACKNOWLEDGMENTS
I should like to express my apprecia-
206 K. N. NESIS
tion: toy Dr. Re Г. Merklin, Dr. Yack
Starobogatov and Prof. P. V. Uschakov
for their help and valuable remarks.
This paper is a modified text of the
report submitted to the 1st meeting on
the investigation of mollusks held in the
Zoological Institute of the Academy of
Sciences of the USSR, Leningrad, at the
end of 1961. It was published in Rus-
sian in the book “Mollusks. The prob-
lems of theoretical and applied mala-
cology” (Moscow-Leningrad, 1964). The
Russian text was kindly translated into
English by Mrs. Г. P. Mokhan'ko and Mrs.
I. P. Penina.
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BELL, A., 1918, The Suffolk boxstones
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ECOLOGY OF CYRTODARIA
ZUSAMMENFASSUNG
ÖKOLOGIE DER CYRTODARIA SILIQUA UND DIE GESCHICHTE
DER GATTUNG CYRTODARIA (BIVALVIA: HIATELLIDAE)
Cyrtodaria siliqua (Spengler) ist von dem nördlichen Ausläufer der Grossen
Neufundland-Bank bis zu der Georges-Bank verbreitet und lebt auf feinem Sand in
Tiefen bis zu 500 m, vorzugsweise von 50 bis 150 m (tiefer als 250 m nur in den
Gebieten mächtiger Wassersenken). Sie wurde von uns bei Temperaturen von 1,0 bis
+5,70 und bei einem Salzgehalt von 32,3 bis 34,2°/oo angetroffen.
Diese Art ist ein beweglicher Sestonophag der losen Böden, dessen Bedürfnisse
in Bezug auf Tiefenlage und Beschaffenheit des Grundes mit seiner Ernährungsweise
verbunden ist. Wahrscheinlich kann sich diese Art bei konstant niedrigen Temperatu-
ren nicht vermehren, infolgedessen fehlt sie nördlich der Grossen Neufundland-Bank.
Nach dem Charakter ihres Areals ist C. siliqua eine nord-boreale westatlantische
Art, nach ihren thermischen Ansprüchen eine niederarktisch-boreale Art.
Die Gattung Cyrtodaria Daudin hat eine atlantische Herkunft. Sie bildete sich um
die Zeit des Übergangs vom Paläogen zum Neogen (ihre Ahnen lebten möglicherweise
im Paläogen in den Meeren der südrussischen Geosynklinale), siedelte sich gegen das
Ende des Neogens in den nordatlantischen und arktischen Untiefen an und zerfiel in
eine Reihe nahe verwandter Arten. In der Folge der Pleistozänvereisungen starben
diese Arten an den europäischen Küsten aus, und die westatlantische С. siliqua wurde
nach Süden zurückgedrängt. In der Periode des postglazialen Klimaoptimums ver-
breitete sie sich nach Norden bis zu den nordöstlichen Küsten Grönlands, konnte aber
nach Island, wo sie in der präglazialen Zeit lebte, infolge der Vertiefung der Däne-
markstrasse, nicht mehr zurück (Nesis, 1961).
Die zweite rezente Art der Gattung, C. kurriana, eine zirkumpolare hocharktische,
an die entsalzten Küstenuntiefen streng gebundene Art, entstand gegen das Pleistozän
in der Arktis. Ihre Ahnen waren ziemlich wärmeliebend und lebten bei normalem
ozeanischen Salzgehalt. In die entsalzten Gebiete war sie durch die mehrmaligen
Entwässerungen der Schelfe infolge der eustatischen Pleistozänregressionen
“hineingetrieben”. Am Anfang der Postglazialzeit (oder in einer der Interglazial-
perioden) verbreitete sie sich nach Süden bis zum Amurliman, starb jedoch in den
Verbreitungs-Mittelpunkten während der nachfolgenden Steigerung der Temperatur und
des Salzgehaltes der Küstengewässer der fernöstlichen Meere aus. Die gegenwärtige
Erwärmung verringert wahrscheinlich ihr Verbreitungsgebiet auch in der Barentssee.
Am Beispiel der Gattung Cyrtodaria kann man zwei Grundwege der Speziation
beobachten: den “Linear- oder Kettentypus” und den “Boukett-Typus” (nach E. F.
Gurjanova, 1951). Die Evolution der Cyrtodaria nach dem “Kettentypus” führte zur
Entstehung der arktischen Art C. kurriana, von wärmeliebenderen Ahnen abstammend
(ein ziemlich seltenes Beispiel einer hocharktischen Art atlantischer Herkunft),
wobei bei allen in der Kette eingereihten Arten die morpho-physiologische Adaptation
an einen bestimmten Nahrungstypus erhalten blieb.
RESUMEN
ECOLOGIA DE CYRTODARIA
Cyrtodaria siliqua (Spengler) se distribuye desde el extremo norte del Gran Banco
de Terranova al Banco Georges, sobre fondos de arena fina hasta 500 m de profun-
didad, pero principalmente entre los 50 y 150 m, y debajo de los 250 m solo se en-
cuentra en areas donde las aguas descienden intensivamente; se ha observado a
temperaturas de -1.0 a -5.7°C y salinidades de 32.3 a 34.2 0/00.
Los requerimientos de profundidad y substrato en esta especie se relacionan con su
tipo de alimentación de substancias móbiles en suspensión. Probablemente no se repro-
duce cuando las temperaturas bajas son constantes, razón por la cual no pasa al
norte del Banco de Terranova. La especie es nor-boreal, del Atlantico occidental y
209
210
К. М. NESIS
sus demandas térmicas del bajo-artico-boreal.
El género Cyrtodaria Daudin es de origen Atlantico. Evolucionö durante la tran-
sición del Paleogeno al Neogeno, de antecesores que vivían principalmente en el
geosinclinal sudprusiano durante el Paleogeno; al final del Eogeno se extendió a los
bajíos del Atlantico Norte y Artico, dividiéndos en un número de especies muy rela-
cionadas. Durante las glaciaciones pleistocénicas las especies desaparecieron de las
costas europeas, y en el Atlantico occidental C. siliqua fue arrastrada hacia el sur.
En el periodo de clima postglacial óptimo se propagó hasta Groenlandia pero debido
al creciente ahondamiento del Estrecho de Dinamarca no pudo esta vez alcanzar Is-
landia, donde ya habia vivido en tiempos preglaciales (Nesis 1961).
La segunda especie viviente, C. kurriana, es circumpolar alto-artica, habitando
sólo las aguas salobres de los bajíos costeros; se originó el Artico al principio del
Pleistoceno. Sus antecesores eran de aguas relativamente cálidas y salinidad nor-
mal. Debido a las repetidas secas de la plataforma durante los periodos de regre-
sión estática, fue acarreado a las aguas salobres. Al principio del postglacial, o en
uno de los interglaciales emigró hacia el Sur tan lejos como el estuario de Amur, pero
en el subsecuente calentamiento y aumento de salinidad de las aguas costeras de los
mares del Lejano Oriente se extinguió en lasareas intermedias. El presente aumento
de temperatura enel Mar de Barents puede también producir eventualmente una reduc-
ción en las distribución de la especie.
El género Cyrtodaria muestra los dos principales tipos en la formación de especies
indicados por E. F. Gurjanova (1951): la “linear o en cadena” y de “ramillete”. La
evolución de Cyrtodaria de acuerdo al tipo “linear” resultó en la transformación de
antecesores que requerian más altas temperaturas (un ejemplo comparativamente raro
de especies Articas de origen Atlantico), en la especie Artica C. kurriana, con cada
especie de la cadena reteniendo las adaptaciones morfofisiolögicas a un tipo definido
de alimentación.
MALACOLOGIA, 1965, 3(2): 211-233
COMPARATIVE FUNCTIONAL STUDIES OF THE DIGESTIVE SYSTEM
OF THE MURICID GASTROPODS
DRUPA RICINA AND MORULA GRANULATA1
Shi-Kuei Wu2
Department of Zoology
University of Hawaii
Honolulu, Hawaii, U. $. A.
ABSTRACT
In the Hawaiian Islands Drupa ricina (L.) occurs in a luxuriant algal environ-
ment, with holothurians and sponges. Morula granulata (Duclos) lives in areas
with less algal growth and occurs with the bivalve Jsognomon and sponges.
The anatomy and histology of the digestive system of D. ricina is described in
detail and compared with that of M. granulata. They are, in general, similar
except with respect to the radula, gland-gut complex, stomach and rectal gland.
D. ricina has 5-cusped rachidian teeth with unindented bases while those of М.
granulata have 3 cusps and an indented rachidian base. Two significant differ-
ences are associated with the gland-gut complex: in D. ricina a pair of sym-
metrically developed accessory salivary glands are free from the mass of the
salivary glands while, in M. granulata, the larger left accessory salivary gland
is completely embedded inthe salivary mass and the right, smaller one, remains
free. The stomachs differ externally: both are essentially a U-shaped sac, but
the stomach of D. ricina has a pouch at the esophageal side, while that of M.
granulata has none. The rectal gland of D. ricina is light yellow and its outline
is obscure, while that of M. granulata is black and easily distinguishable ex-
e ternally.
The functional aspects of the digestive system of D. ricina and М. granulata
are discussed. The buccal cavity, salivary glands and their accessory glands
are associated with lubrication during feeding. Ciliary currents occur through-
out the entire digestive system except in the buccal cavity.
Morula was observed to drill bivalves, though it preferred carrion, while
Drupa is not thought to be a typical predator of hard-shelled mollusks, but to
subsist on live prey, such as sponges and holothurians, or carrion. The feeding
habits and dietary differences are placed in relation with the structural differ-
ences in the digestive system. Comparison of the feeding habits and stomach
patterns of Drupa and Morula with that of carnivorous Mesogastropoda and other
Stenoglossa seems to indicate that Drupa and Morula represent the basal or
primitive features of the Stenoglossa, reflecting their mesogastropod ancestory.
INTRODUCTION well known for their predatory habits.
Despite numerous studies on various
The muricid gastropods (superfamily aspects of the digestive system (radula:
Muricacea, suborder Stenoglossa) are Cooke, 1919; Arakawa, 1957, 1958,
Lrhesis submitted to the Department of Zoology of the University of Hawaii in partial fulfilment
of the requirements for the degree of Master of Science.
2Present address: Institute of Zoology, Academia Sinica, Nankang, Taipei, Taiwan, Republic
| of China.
(211)
212 5. К. WU
1962а; proboscis: Herrick, 1906;
Carriker, 1943; esophagus.and stomach:
Graham, 1941, 1949; mid-gut gland:
Nakajima, 1956; and fecal pellets:
Arakawa, 1962b) there is no compre-
hensive functional study of the digestive
system of any muricid. The purpose
of this paper is to report on a compara-
tive functional study of the digestive
system of 2 muricids: Drupa ricina (L.)
and Morula granulata (Duclos).
D. ricina and M. granulata are both
readily available in the littoral zone of
the Hawaiian Islands. Previous work
on Drupa and Morula is limited to the
taxonomic studies by Burch (1955), Dall
(1923, 1924), Hedley (1913) and Hertlein
(1960), the report on spawning and
development of Morula by Ostergaard
(1950), and the radular study by Cooke
(1919).
MATERIAL AND METHODS
Specimens of р. ricina and М. granu-
lata were collected at Black Point,
Waikiki, and Kewalo, Oahu, and dissected
both alive and after preservation. For
histological studies the digestive system
of the snails was cut into the following
parts: 1) proboscis, 2) gland-gut com-
plex (including the organ of Leiblein3,
nerve ring, mid-esophagus, salivary
gland and its accessory gland) and the
gland of Leiblein, 3) stomach and di-
gestive gland, and 4) intestine and
rectum. Fixatives for histological
preparations included Bouin’s, 5%
neutral formalin and Flemming-without-
acetic-acid. Paraffin sections were cut
at 5 - 8 и. Three staining methods:
Delafield’s hematoxylin and eosin, Mal-
lory’s triple stain, and Heidenhain’s
iron-hematoxylin, were utilized for
specimens fixedin Bouin’s and 5%neutral
formalin. Mallory’s triple stain was
The term is combined from “pharynx of
Leiblein” and “pyriform organ” (Graham,
1941) and “valve of Leiblein” (Fretter &
Graham, 1962).
especially useful for descriptions ofboth
nuclear and cytoplasmic structures.
Tissues fixed with Flemming-without-
acetic-acid were stained in safranin and
light green, a technique utilized by
Millot (1937).
Radulae were fixed and flattened in
70% ethyl alcohol, dehydrated and
mounted in Euparal.
Observations of ciliary currents were
made by the direct method of injecting
fine particles of either carmine or India-
ink on to the excised gut, and by the
indirect method of examininghistological
preparations, as adopted and discussed
by Millot (1937).
FUNCTIONAL MORPHOLOGY OF THE
DIGESTIVE SYSTEM OF
DRUPA RICINA (L.)
Habitat and external features
D. ста (Pl. I, Fig: 1) occurs if
the inter-tidal zone of the rocky shore,
or of a sand shore studded with rocks,
where Ulva fasciata and other algae
grow abundantly. The snails cling to
the undersurfaces and sides of large
rocks which have relatively smooth
surfaces. Associated with D. ricina
are a holothurian, Holothuria atra, and
the mollusks Cypraea caputserpentis,
Aplysia juliana and, with minor eco-
logical differences, Morula granulata
and М. nodus.
D. vicina is readily distinguished by
its solid, biconical, low-spired shell,
the surface of which is tuberculated.
The shell itself is primarily yellow-
green but is usually covered with vari-
ously colored calcareous algae and may
be white or purple red.
The head and foot of D. ricina are
different shades of green, mottled with
white or black. The 2 long tentacles
and the anterior siphon are seen when
the snail is moving about. The foot is
more or less lanceolate, somewhat bi-
lobed in front, angulated at each corner,
and rounded or bluntly pointed behind.
The ventral creeping surface is milky-
DIGESTIVE SYSTEMS OF TWO MURICIDS
green and is grooved medially. Im-
mediately behind the anterior margin
of the foot is a transverse groove in
the anterior 1/6th of the foot. A horny
operculum rests on the posterior end of
the dorsal surface of the foot. The
operculum has an eccentric nucleus and
is of the lamellate type.
Anatomy and histology of the
digestive system
The buccal region. The mouth (M)
lies at the summit of a long pleur-
embolic proboscis (PR). Itis oval with
two-fold lips and immediately at the
inner border of the lip the dorsal and
ventral jaws are distinguishable. The
dorsal jaw or “sclerite” (Carriker, 1943)
is a beak-like structure. The transverse
section of the dorsal jaw (DJ) shows
2 prominent lateral elevations (LE) and
a low central elevation (CE) (Pl. I, Fig.
1). The central elevation rapidly
vanishes posteriorly, where a central
depression forms a dorsal groove (DG)
between the 2 lateral elevations (Pl. III,
Fig. 4).* The ventral jaw (VJ) is rec-
tangular, with its long axis in antero-
posterior direction; it also has2lateral
elevations (LE) and a concave surface
between these elevations. Furrows (FU)
are present (Carriker, 1943)between the
lateral walls of the buccal cavity and
the lateral elevations of the dorsal and
ventral jaws (Pl. II, Fig. 1).
The odontophore (O) is composed of
the retractor muscles, 2 cartilagenous
rods (CR) and the radular sac (RS). The
latter, together with its membrane,
covers these 2 complex masses of
muscles and cartilage projecting an-
teriorly into the buccal cavity (BC).
Posteriorly the radular sac runs below
the anterior esophagus (AE); it has a
coiled free blind end.
The buccal cavity is lined with a
“Since the anatomy of D. ricina and M. granu-
lata, are, in general, very similar, sections
of the latter species are occasionally quoted
to illustrate features discussed in the
former.
213
columnar epithelium, the cells of which
have oval nuclei located in the center
of the cell. The dorsal wall is dis-
tinguished by a pair of dorsal folds (DF)
equipped, especially medially, with long
cilia which beat toward the dorsal groove
(DG) (Pl. III, Fig. 4). The ventral wall
is formed by the ventraljaw. The lateral
walls are covered by a thin cuticle
(LCU) which is continuous with the dorsal
and ventral jaws.
The ducts of the salivary glands open
into the buccal cavity at the lateral side
of the ventral jaw (VJ). An extremely
small, single duct of the accessory
salivary glands opens mid-ventrally to
the outer surface of the lip.
The radula is of the rachiglossate type
usually formulated as 1-C-1 (Pl. I, Fig.
2). The rachidian or central tooth (RT)
possesses 5 main cusps, of which the
central cusp (CC) is the longest one.
Each of the 2 lateral cusps (LC) has
denticles (MD, LD) medially and later-
ally. The marginal cusps (MCU) are less
than half the length of the lateral cusps
(LC). The tips of all cusps are sharply
pointed. The anterior margin of base (В)
of the rachidian is concave, but projects
slightly at the median, thus forming 2
waves. Thelateraltooth (LT)istypically
sickle-shaped with a thick, broad base
and an extremely long process which
reaches half way over the next tooth in
the radular row. All the teeth rest on
a membrane of connective tissue.
The esophageal region. The esopha-
geal region is extremely long and compli-
cated. Itis most conveniently divided into
3 parts: the anterior, mid-, and pos-
terior esophagus (Graham, 1941).
The anterior esophagus (AE, Pl. I)
begins above the opening of the radular
sac and ends before the organ of Leiblein.
Its dorsal folds (DF) are the contin-
uations of the prominent dorsal folds of
the walls of the buccal cavity (BC, Pl. Ш,
Fig. 4). The tract between the folds is
the food channel (FC), the outline of which
is transversely H-shaped (Pl. II, Fig. 4b).
As the anterior esophagus terminates,
the dorsal folds diminish and several
214 S. K. WU
JD
wn
x
ot eee Ts
y
------
=
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TU
FIG. 1. Drupa ricina; apertural view of shell.
FIG. 2. Drupa ricina; dorsal view of the digestive system.
FIG. 3. Drupa ricina; dorsal view of the digestive system, except for proboscis and convoluted
portion of mid-esophagus, which are shown laterally, with the glandular structures
removed. Lower-case letters a-k refer to transverse sections on Pl. II, Fig. 4.
DIGESTIVE SYSTEMS OF TWO MURICIDS
equally developed, more or less sym-
metrical folds appear (Pl. II, Fig. 4c).
Histologically the anterior esophagus
is lined with ciliated columnar cells with
central, oval nuclei.
215
The cytoplasm of
the distal ends of the cells stains deeply
with eosin.
The cilia are especially
well developed on the dorsal folds.
KEY TO LETTERING IN PLATES
anus
anterior aperture of the digestive duct
almost circular fold
anterior esophagus
aperture of LGD
ampulla of the gland of Leiblein
accessory salivary gland
artificial space
base of the rachidian tooth
buccal cavity
cilia
central cusp
cilia cell
central elevation
connective tissue and muscle
convoluted portion
cartilaginous rod
connective tissue
denticle
“digestive” cell
dorsal fold
dorsal groove
digestive gland
dorsal jaw
esophageal region of stomach
major fold of stomach
minor fold of stomach
food channel
food groove
furrow
gonad
granules
glandular epithelium of the organ of
Leiblein
gastric shield region
inner epithelial layer
intestinal groove
intestine
lumen
left accessory salivary gland
lateral cusp
lateral cuticle
lateral denticles of the lateral cusp
lateral elevation
the gland of Leiblein
duct of the gland of Leiblein
the organ of Leiblein
lateral tooth
mouth
mucoid cell
marginal cusp
medial denticle
middle muscular layer
mucous pad
mucus
nucleus
nucleus of cilia cell
nucleus of epithelial cell
nucleus of mucoid cell
nerve-ring portion
odontophore
outer glandular layer
pouch
posterior aperture of the digestive
duct
posterior esophagus
phagocyte
proboscis
rectum
right accessory salivary gland
rectal gland
radular sac
rachidian tooth
“secretory” cell
salivary duct
salivary gland
style sac region
stomach
major typhlosole
minor typhlosole
ventral cleft of the organ of Leiblein
ventral fold
ventral groove
ventral jaw
216
FIG. 1.
FIG. 2.
FIG. 3.
See WU
PLATE I
Drupa ricina; a transverse section through the anterior portion of the buccal cavity.
Drupa ricina; radula.
Drupa ricina; a series of semidiagrammatic frontal sections through the organ of
Leiblein at the points a, b, c, marked by arrow-heads in Pl. II, Fig. 4d.
DIGESTIVE SYSTEMS OF TWO MURICIDS 217
Scattered among the ciliated cells are
mucus cells. The esophagus is sur-
rounded by circular musclesin which the
ducts of the salivary glandare embedded.
The mid-esophagus begins with the
organ of Leiblein (LO) and extends to the
point of entrance of the duct of the gland
of Leiblein (LGD). The mid-esophagus
can be subdivided into 3 portions on the
basis of prominent structural differ-
ences: the organ of Leiblein (LO), the
nerve-ring portion (NRP), and the con-
voluted portion (CP, Pl. I, Fig. 3). The
organ of Leiblein is a markedly pear-
shaped expansion of the esophageal tract,
the apex of which points posteriorly and
ventrally, because of the ventrally
located nerve ring which has pulled down
on the digestive tract. The organ of
Leiblein is opaque white except for a
dark streak curving around the organ. It
starts at the midventral line on its an-
terior side and comes to lie on the right
Side at the posterior end of the organ.
The streak is dueto an extremely narrow
cleft (V) in the tissue of the wall, ex-
panding into a hernia-like protrusion of
the lumen (Pl. II, Figs. 4d € 4e). Because
of the extreme thinness of the glandular
epithelium (GE) at this point, the cavity
oí the esophagus can be seen through it
as a shadow (Graham, 1941).
An almost circular mucus pad (MP)
lies in the wall of the organ, excepting at
the midventral cleft (У) (Pl. II, Figs. 4d
€ 3a) and forms the base of an almost
circular fold (ACF), the ciliated lip or
valve of Graham's (1941) terminology,
projecting into its cavity (Pl. II, Figs.
3b, 3c and 4d). The right side of the
mucus pad is located slightly anterior to
the left one (Pl. II, Fig. 3a), a con-
figuration probably due to torsion. His-
tologically, 2 types of cells are present
(Pl. II, Fig. 3). One type consists of
mucoid cells (MC) which have round or
oval nuclei (NM) placed closely against
the basement membrane. The second
type includes those cells bearing cilia
(CCE) which have elongated nuclei (NC)
located 1/3 of the distance from the
apical end of the cells. The base of the
cells is thread-like, reaching the base-
ment membrane. The apical end of the
cytoplasm stains slightly andis striated;
this striation connects with the cilium
of each cell. The anterior side of the
almost circular fold is lined with ex-
tremely long ciliated, columnar epi-
thelial cells and the posterior side is
lined with columnar cells which stain
lightly. The remaining portion of the
organ of Leiblein consists of glandular
epithelium (GE, Pl. II, Fig. 3) which
stains deep blue with Mallory’s triple
stain. Here there are also 2 types of
cells similar to those of the mucus pad
except that the cytoplasm stains much
more densely.
The bottom of the narrow, hernia-like
cleft is lined with squamous Cells without
cilia. The lateral wall is lined with
ciliated columnar cells which decrease
both in height and in length of cilia as
they approach the bottom of the cleft.
The organ of Leiblein is coated by fibrous
connective tissue which contains a layer
of muscle fibers.
Posterior to the organ of Leiblein the
mid-esophagus becomes extremely
narrow and curves slightly to the left
side of the medial axis where it is sur-
rounded by the nerve-ring and can thus be
referred to as the nerve-ring portion
FIG. 4. Drupa ricina; a series of diagrammatic transverse sections through the digestive
canal at the points a-k marked by arrow-heads in Pl. I, Fig. 3.
a. Through the junction of the buccal cavity and the anterior-esophagus. B. Through
the anterior part of the anterior esophagus. c. Through the posterior part of the an-
terior esophagus. d. Through the anterior part of the organ of Leiblein. e. Through
the posterior part of the organ of Leiblein. f. Through the nerve ring portion of the
mid-esophagus.
g. Through the convoluted portion of the mid-esophagus. h. Through
the posterior esophagus. i. Through the duct of the gland of Leiblein. j. "Through the
intestine. k. Through the rectum.
218 5. К. WU
(NRP, Pl. I, Fig. 3). The epithelium of
this region is folded into longitudinal
ridges and grooves. The dorsal side is
greatly modified as the dorsal fold (DF,
Pl. I, Fig. 4f) in which the epithelial
cells are mainly mucoid (MC, Pl. V, Fig.
1) staining light blue in Mallory’s triple
stain. Numerous phagocytes are between
the mucoid cells. The ventral side of
the tract consists of ridges and grooves.
These are lined with ciliated columnar
epithelial cells, the apical ends of which
stain more deeply than the basal ends.
The nucleus is round and centrally
located. The nerve-ring portion is coated
with fibrous connective tissue which con-
tains embedded muscle fibers.
Posterior to the nerve-ring portion,
the mid-esophagus gradually shifts to the
right side of the medial axis of the
animal and upwards, at the same time
expanding into a large tube greater in
diameter than any other part of the
esophagus; this is due to the expansion
and convolution of the dorsal wall (the
“median unpaired fore-gut gland” of
Haller [1888], the “glande framboisée”
of Amaudrut [1898], or the “convolution”
of Graham[ 1941]. The convoluted portion
(CP) is completely hidden under the gland
of Leiblein (LG, Pl. I, Fig. 2)and extends
as far back as the point at which the
duct of the gland of Leiblein enters on
the right side. The histology of this
portion is similar to that in the nerve-
ring portion, except that the dorsal fold
is much more developed than formerly.
The degree of modification of this portion
varies with individual specimens. The
convoluted portion is coated, as is the
former portion, with fibrous connective
tissue containing embedded muscle
fibers; these fibers are thicker than
formerly, averaging 30 „ in thickness.
The posterior esophagus (PE, Pl. I,
Figs. 2 & 3) is slender and long. In
cross section (Pl. II, Fig. 4h) about 10
equally developed longitudinal folds can
be observed. Histologically the posterior
esophagus is similar to the nerve-ring
portion of the mid-esophagus.
Three glands are associated with the
esophagus; the paired salivary and
accessory salivary glands (SG, ASG),
which open into the buccal cavity, and
the unpaired gland of Leiblein, which
opens into the mid-esophagus.
The salivary glands. The salivary
glands area white mass, which surrounds
the organ of Leiblein and is overlapped
by the gland of Leiblein on the dorso-
posterior side. The mass cannot be
macroscopically recognized as a bi-
lobed structure, but when the branching
system of ductules is traced, it is evi-
dent that it is acutally composed of 2
closely approximated lobes. Each lobe
is of the compound acinous type. The
cells of the terminal portion are of 2
types (Pl. IV, Fig. 1). Mucoid cells
(MC) are most numerous. The oval
nucleus (N) is centrally located; and
the cytoplasm stains blue with Mallory’s
triple stain. “Secretory” cells (SC) are
less numerous than mucoid cells; they
are triangular in shape, with an oval
nucleus located basally; the cytoplasm
is filled with equal-sized granules which
stain red with Mallory’s triple stain.
The duct system of the salivary gland
is of the dichotomous branching type.
The ductules are approximately 30 - 40
у in diameter. The ductules of each gland
finally converge into a single duct which
leaves the gland near the anterior region
of the organ of Leiblein and runs an-
teriorly along the dorsal folds of the
anterior esophagus (SD, Pl. II, Figs. 4b
& 4c). At the junction of the anterior
esophagus and the buccal cavity the
duct descends and penetrates the ventro-
lateral walls of the buccal cavity. The
diameter of the duct averages 75 y. It is
lined with low epithelial cells, 7 „ in
height (Pl. IV, Fig. 2), whose oval nuclei
(NEC) possess clear nucleoli and whose
cytoplasm stains lightly with eosin. The
cilia (C) are long and form bundle-like
structures, whose origins are concen-
trated near the nucleus.
The accessory salivary glands. The
accessory Salivary glands (ASG, Pl. I,
Fig. 2) are a pair of tubular structures
which are located laterally to the nerve
DIGESTIVE SYSTEMS OF TWO MURICIDS 219
ring. The terminal portion of the left
gland swells posteriorly, while that of
the right gland swells anteriorly. A
transverse section of the gland shows
that it is divided into 3 layers (Pl. IV,
Fig. 3). The outer layer (OGL), which
is the thickest of the 3, consists entirely
of mucoid cells. These cells are tall
columnar cells with long necks which
penetrate the next 2 layers and open
into the lumen (L) of the gland (not shown
in figure). The nuclei of these mucoid
cells are small, round, and centrally
located; the cytoplasm stains homo-
geneously deep-blue with Mallory’s
triple stain and pink with eosin. The
middle layer (ММГ) consists of circular
muscle fibers, between which inter-
penetrate the necks of the mucoid cells
mentioned above, and some connective
tissue. The inner layer (IEL), which
lines the lumen, is composed of low
columnar epithelial cells with round or
oval nuclei. These cells surround the
terminal necks of the mucoid cells.
The proximal portion of each tubular
gland is coiled and gradually decreases
in diameter. The proximal tubes from
right and left join anterior to the nerve-
ring, forming an extremely fine duct
which runs below the hemocoel of the
proboscis. The duct is lined with
cuboidal cells, having oval nuclei, dis-
tinct nucleoli and lightly staining cyto-
plasm. The duct opens to the outer
margin of the inner lip. The diameter
of the duct near the opening is about
25 u.
The gland of Leiblein. The gland of
Leiblein (LG, Pl. I, Fig. 2)is a single,
large, brown or yellow mass which lies
immediately behind the salivary gland
mass and overlapsthe convoluted portion
(CP) of the mid-esophagus. It is tall
and triangular with a terminal position
ampulla (AM). The left side of the gland
has 2 anterior-oblique incisions.
The gland is of the monopodial
branching type. Each terminal portion
consists of 2 types of cells: “granular”
and mucoid (Pl. IV, Fig. 4). The
“sranular” cellsare columnar cells with
round or oval nuclei which appear in the
basal portion of the cell in hematoxylin-
eosin stained material. The nucleus is
not visible when using Mallory’s triple
stain because of the presence of gran-
ules. At the proximal portion of the
cell the granules (GR) are smaller and
stain red to orange, while in the distal
half of the cell the granules are larger,
stain blue to green, and are surrounded
by vacuoles. Mucoid cells (MC) are
scattered among the “granular” celis.
Each lobule of the gland has a ventral
fold and groove which convergestowards
the single duct of the gland. The duct
is short (about 1 - 2 mm) and opens
into the mid-esophagus from the dorsal
side. The duct wall on the oral side
of the duct is formed by the continuation
of the convoluted portion of the mid-
esophagus. However, as it approaches
the gland of Leiblein, the glandular cells
are greatly reduced in number and the
epithelium is formed of a cuboidal cell
layer. The opposite wall, which is lined
with tall ciliated columnar cells, bears
the ventral folds of the duct (VF, Pl. II,
Fig. 4i) Here the apical ends of the
cell stain deeply. A deep groove is
formed between the folds, the cells of
which stain lightly.
The stomach. The stomach (ST) is
a U-shaped sac with a distinct pouch (P)
at the esophageal end of the base of U
(Pl. I, Figs. 2 & 3). In surface view the
dorsal side of the stomach is visible;
the major portion of the stomach is
covered by the other viscera, such as
the kidney, digestive gland (DGL) and
gonad (G). The long posterior esophagus
opens into the esophageal region of the
stomach (ER, Pl. V, Fig. 4); the intestine
leaves the stomach from the right angle
of the U-sac.
Internally, the stomach (Pl. V, Fig. 4)
is a simple sac with 2 longitudinal folds
more or less continuous with the typhlo-
soles of the intestine. These separate
the intestinal groove (IG) from the
stomach proper. The major fold (F1)
bordering this groove, arises at the
junction of the posterior esophagus and
220 5. К. WU
PLATE Ш
FIG. 1. Morula granulata; apertural view of shell.
FIG. 2. Morula granulata; dorsal view of the digestive system.
FIG. 3. Drupa ricina; a part of the mucus pad and the glandular epithelium of the organ of
Leiblein.
FIG. 4. Morula granulata; atransverse sectionthrough the position region of the buccal cavity.
FIG. 5. Morula granulata; radula.
DIGESTIVE SYSTEMS OF TWO MURICIDS 221
the stomach; it follows the curve of
the stomach, flattening out andbecoming
less distinct posteriorly. In the style
sac region it is continued by the typhlo-
sole (T1). The minor longitudinal
stomach fold (F2) similarly arises and
runs parallel to the major fold, finally
continuing as the minor typhlosole (T2)
in the style sac region.
The stomach proper can be divided
topographically into an anterior esopha-
geal region (ER), a “gastric shield”
region (GSR) and a posterior style sac
region (SSR) (Pl. V, Fig. 4). In the
esophageal region a series oftransverse
parallel ridges and grooves runs across
the stomach at right angles to the major
fold. The region just before the pos-
terior end of the style sac is smooth-
walled, and the major fold is less
prominent than in the esophageal region.
Although neither a gastric shield, suchas
occurs in the stenoglossans (e.g. Cyclope
neritea; Morton, 1960), nor a cuticular
epithelium indicating its remnant, were
observed; this distinct region is here
called the gastric shield region for
reasons of analogy. The style sac region
(SSR) commences near the posterior
aperture of the digestive duct (PAD) and
ends at the intestine (INT). In the style
sac region the typhlosoles (T1 and T2)
meeting the stomach folds become
distinct. The wall here shows weak
ridges and grooves which are Set at
right angle to the typhlosoles. In dis-
secting one living specimen, a “proto-
style” or mucus rod (Graham, 1939)
was obtained in the style sac region.%
The intestinal groove (IG), a de-
pression in the floor of the stomach,
runs, at first between the major and
the minor stomach folds and later
between the typhlosoles, from the
esophageal angle of the stomach to the
intestine. Two apertures of the di-
gestive gland open into this groove: the
anterior aperture (AAD) opens at the
esophageal angle of the stomach, the
posterior aperture (PAD) opens at the
SThat a protostyle was found only once may
perhaps be due to rapid dissolution before
dissection.
height of the “gastric shield” region.
The stomach is lined by a ciliated
columnar epithelium the cells of which
average 40 y in height. The epithelium
of the longitudinal gastric folds and of
the transverse ridges of the esophageal
region of the stomach have especially
tall columnar cells. The height of the
cells in these regions averages 90 u.
In all the epithelial cells there are
elongate nuclei which are centrally
located. The cytoplasm stains homo-
geneously except for the apical end of
the cells where it stains somewhat more
densely. The cilia are 10 „ in length
throughout the stomach epithelium.
Mucus cells are scattered among the
columnar epithelial cells. At the base
of the epithelial cells there are infiltrated
phagocytes which possess oval or round
nuclei that stain red with Mallory’s
triple stain. Below the epithelium are
dense fibers which stain deep blue with
Mallory’s triple stain. Embedded in
the connective tissue are blood cells,
fibroblasts and muscle fibers. Blood
spaces are located between the digestive
gland and the stomach.
The digestive gland. The digestive
gland (DGL, Pl. I, Fig. 2) is a brown
mass which surrounds all ofthe stomach
except for its dorsal surface. It coils
in a counterclockwise direction together
with the stomach and the gonad.
The digestive gland is of the compound
acinous type. Two types of cells are
present: “digestive” and “secretory”.
The “digestive” cells (DC, Pl. IV, Figs.
5 & 6) are more numerous and are
columnar epithelial cells. Their nuclei
are round or oval and are located in
the basal portion of the cells. Thecyto-
plasm is filled with granules which stain
red, yellow-green and blue with
Mallory’s triple stain. The red granules
occur inthe proximal portion, the yellow-
green in the middle, andthe blue granules
in the distal portion of the cells. The
blue granules are surrounded by a
vacuole. All the granules stain black in
Heidenhain’s iron-hematoxylin.
The “secretory” cells (SC) are tri-
angular in a longitudinal section with a
broad surface along the base of the
222 5. К. WU
epithelium. They taper to a fine point
(Pl. IV, Fig. 6) where they reach the
lumen of the tubule. The “secretory”
cells tend to occur in groups at the
distal ends of tubules where the cells
face the visceral hemocoel. The nuclei
are round or oval and are relatively
smaller than those of the “digestive”
cells. The cytoplasm stains densely.
The terminal portion of the gland is
coated withathin connective tissue mem-
brane. The space among the tubules is
usually filled with blood corpuscles which
are oval and which have round or oval
nuclei.
The duct of the digestive gland is of
the dichotomous branching type and opens
into the stomach by way ofthe 2 apertures
discussed above. The duct is a con-
tinuation of the stomach epithelium, and
is histologically identical with that of the
stomach walls, consisting of a lining of
ciliated columnar cells.
The intestine. The intestine (INT,
Pl. I, Figs. 2 & 3) leaves the stomach
at the end of the style sac region. It
runs parallel to the posterior esophagus
as far as the region of the heart and
then continues ventrally to the heart,
shifts laterally and dorsally under the
kidney, and eventually leads into the
dorso-ventrally compressed rectum.
The intestinal wall is rather smooth,
bearing the major and minor typhlosoles
leading out from the stomach. These are
prominent in the proximal portion óf the
intestine only and gradually disappear
(Pl. I, Fig. 4j). The intestine is lined
with a ciliated columnar epithelium. The
nuclei are ovaland more or less centrally
located; the cytoplasm stains deeply at
the apical end of the cells. Mucoidcells
are scattered among the epithelial cells
but are not numerous. The intestine is
coated with thin connective tissue.
The rectum. The rectum (R, Pl. I)
begins where the intestine is dorso-
ventrally flattened. The wall of the
rectum (Pl. II, Fig. 4k) is longitudinally
folded; the folds are conspicuously better
developed than in the intestinal wall. The
histology is similar to that of the
intestine.
The anus (A) opens into the right
corner of the mantle cavity and termi-
nates in a papilla-like projection, about
7 mm from the mantle margin. The wall
of the anus is distinctly folded into
ridges and grooves.
The rectal gland. The rectal oranal
gland (RG, Pl. I, Fig. 2) which is wedged
between the rectum, the mantle and the
hypobranchial gland, is а _ branching
tubular structure which opens into the
rectum near the anus. It is not well-
developed, very pale yellow in color and
is usually difficult to perceive in dis-
section.
Feeding and ciliary currents
Feeding. Unfortunately field and the
laboratory observations failed to eluci-
date the feeding habits of D. ricina.
Examination of the stomach contents
revealed: the complete exoskeleton of
young shrimp, a young holothurian,
sponge spicules, flagellates, andseveral
kinds of algae (mainly diatoms and fila-
mentous green algae). These obser-
vations seem to indicate that D. уста
is not a typically mollusk-drilling,
predatory species but rather that it
subsists on a varied diet, perhaps in-
cluding carrion. Though neither feeding
habits nor the feeding mechanism have
been determined, the stomach contents
suggest that sucking may possibly be
involved in the feeding mechanism. The
hypothesis that sucking may play a part
in feeding is given further weight by
observation of some ciliary currents in
the buccal cavity in livingexcised speci-
mens. Althoughtransference ofparticles
falling on the tip of the proboscis and
the ventral wall of the buccal cavity to
the esophagus was almost negligible in
the buccal cavity proper, distinguishable
ciliary currents were noted at the
junction of the buccal cavity and the
anterior esophagus.
Ciliary currents. Ciliary currents
in the anterior esophagus result largely
from ciliary action of cells onthe dorsal
folds (DF, Pl. V, Fig. 3). The particles
DIGESTIVE SYSTEMS OF TWO MURICIDS 223
are entangled by mucus secreted by the
mucoid cells. Within a few seconds the
particles and mucus form a fine string,
the food bolus, which is slowly moulded
and transported posteriorly. Weak
peristaltic contraction initiating from the
anterior end of the esophagus and
spreading posteriorly may aid in the
movement of the food materials.
At the end of the anterior esophagus
the food bolus is passed through the
canal of the almost circular fold to the
main cavity of the organ of Leiblein.
The particles moving toward the canal
situated below the narrow cleft (V, Pl.
Il, Fig. 4d) are lifted upward and in-
corporated into the food bolus. In the
organ of Leiblein the cilia of the almost
circular folds move back and forth in
the excised specimens.
The particles falling on the glandular
epithelium (GE) of the organ of Leiblein
move down to the ventral medial food
groove (FG) (Pl. II, Fig. 4e;, see also
Pl. V, Fig. 3). Histological studies also
indicate that the cilia of the glandular
epithelial cells move toward the ventral
Side, as does the occurence of mucus in
the cavity. The epithelial cells around
the groove stain light blue in Mallory’s
triple stain and may be an interesting
feature of the mucus secretion phase.
The narrow hernia-like cleft was free
from food at all times; its function
was not determined.
The food string moves from the
organ of Leiblein posteriorly into
the nerve-ring portion of the esopha-
gus. While it moves along the ventral
surface of the tube, particles which
fall into the dorsal groove are re-
jected and swept obliquely-laterally
over the fold and to the. sides where
they move posteriorly.
In the convoluted portion the ciliary
currents are similar to those in the
nerve-ring portion.
In the posterior esophagus the food
bolus is passed posteriorly and receives
the string-like secretion of the gland of
Leiblein (Pl. V, Fig. 3). This latter is
incorporated into the food bolus,
Spiralling into the bolus in a clockwise
direction (anterior view).
The ciliary currents in the stomach
(Pl. V, Fig. 4) move the food in a
clockwise spiral fashion in the stomach
proper (i.e. not into the intestinal
grove). A fewgrooves which run parallel
to the major gastric fold move it pos-
teriorly toward the “gastric shield
region”. Thus the food bolus in the
stomach is formed by the rotatory move-
ment of the cilia of the stomach epitheli-
um.
Particles falling into the intestinal
groove are rejected by way of the tiny
ridges and grooves in the intestinal
groove itself. Some particles move
along the inner edge of the minor stomach
fold together with secretions from the
digestive gland and go into the intestine.
Particle movement in the intestinal
groove is especially rapid.
The food bolus in the stomach proper
is gradually passed over to the gastric
Shield region. Rotation is also ina
clockwise direction. The particles move
Slowly here. A complete holothurian
was found in this region. The foodbolus
passes eventually into the style sac
region, and the bolus is further mixed
with the secretion of the epithelial cells
here.
In the intestine the food bolus is
rotated and mixed with the secretions
of the digestive gland which are intro-
duced by way of the intestinal groove.
Once the food bolus has reached the
rectum, movement is slowed down and
the ciliary currents here indicate that
the food bolus and stray particles are
moved back and forth in the same
position. The feces are formed at the
distal end of the rectum and finally
are passed outside through the anus.
The feces contain many kinds of diatoms,
filamentous green algae, sponge spicules
and different sizes of sand grains.
FUNCTIONAL MORPHOLOGY OF THE
DIGESTIVE SYSTEM OF
MORULA GRANULATA (DUCLOS)
Habitat and external features
М. granulata occurs in the intertidal
224 S. K. WU
PLATE IV
FIG. 1. Morula granulata; a portion of transverse section of the tubules of the salivary gland.
FIG. Morula granulata; a transverse section of the duct of the salivary gland.
FIG. 3. Morula granulata; a portion of transverse section of the accessory salivary gland;
semi-diagrammatic: shown are the 3 layers, but not the fact that the mucoid cells of
the first layer penetrate the 2 other layers.
FIG. 4. Drupa ricina; a portion of the epithelium of the gland of Leiblein.
FIG. Drupa ricina; a portion of transverse section of the tubule of the digestive gland.
FIG. 6. Morula granulata; a portion of longitudinal section of the distal end of the digestive
gland tubule.
The scales of Figs. 1, 4, 5 and 6 are at Fig. 5.
D
A
DIGESTIVE SYSTEMS OF TWO MURICIDS
zone of the sand-rocky shore and on coral
reef flats. Those snails which live along
the sand-rocky shore wedge themselves
in crevices and between boulders. Those
snails which live on the reef flat occur
on the undersurface of rather smooth
coral fragments or rock. There M.
granulata occurs with /sognomon, а
lamellibranch which is attached to the
coral blocks by byssal filaments.
Numerous empty /sognomon shells were
observed near specimens of M. granu-
lata.
The shell of М. granulata (Pl. Ш, Fig.
1) is solid and biconical, and its surface
is granulated. The shell is black but it
is usually encrusted with variously
colored calcareous algae.
The head and body of M. granulata
are similar to those of D. ricina except
for coloration: the exposed soft parts
are black.
Anatomy and histology of the
digestive system
The anatomy andhistology of M. granu-
lata are, in general, similar to those of
р. vicina. In the following account
attention will be focused chiefly on
differences of detail, especially with
respect to the radula, gland-gut com-
plex, stomach and rectal gland.
The radula formula is also 1-C-1.
The rachidian tooth (RT, Pl. Ш, Fig. 5)
possesses 3 main cusps of which the
central cusp (CC) is the longest. The
central cusp is sharply pointed while
the lateral cusps (LC) have a strong
medially placed denticle (D) which is
free from the lateral cusp. There are
2 blunt denticles or rather wrinkles
lateral to the lateral cusps. The angles
of the margins are somewhat raised but
do not form cusps. The base (B) of the
rachidian is rectangular and has an
indentation or pit on the posterior side,
which serves to anchor the cusps. The
lateral teeth (LT) are typically sickle-
shaped, like those of D. vicina, but much
more slender and smaller in size.
The left accessory salivary gland is
completely embedded in the salivary
225
gland while the right accessory salivary
gland is free from it. The pair is
asymmetrically developed, the right
accessory Salivary gland being smaller
than the left one. In spite of the
difference in development, the histo-
logical structure of the accessory sali-
vary gland is similar to that of D. уста.
The stomach of M. granulatais almost
entirely embedded in the digestive gland
(DG) except for a portion which, in
dorsal view, shows externally as a U-
shaped tube (Pl. Ш, Fig. 2). Asin D.
vicina the stomach is a U-shaped sac,
but it lacks the pouch at the base of the
U. Its internal structure (Pl. V, Fig. 5)
is similar to that of D. rzcina.
The epithelial folds of the intestine are
slightly less developed in M. granulata.
The location of the rectal gland corre-
sponds to that in D. vicina, but it is
well developed and can be easily seen
by its black coloration. It isabranching
type of gland from whose main trunk
long branches emerge laterally and short
branches emerge medially (Pl. III, Fig.
2). Histologically the transverse sec-
tions of the trunk and branches of the
rectal gland (Pl. V, Fig. 2) are lined
with ciliated, low columnar cells. The
nuclei (N) are round or oval and centrally
located. The cells mainly contain large
brown to black granules (GR) which give
rise to the black color of the gland.
The cytoplasm is homogeneously and
lightly stained. The apical ends of the
cells stain light blue in Mallory?s stain.
The rectal gland is coated by a thin
fibrous membrane and some muscle
fibers are attached to the membrane. It
is also surrounded by fatty tissue, as
is the rectum.
Feeding and ciliary currents
Feeding. In both the field and the
laboratory М. granulata clings to 2
species of /sognomon, I. incisum and J.
costellatum, and feeds on them, either
by actually boring or by projecting the
proboscis through the slit between the
valves of the lamellibranch. M. granu-
lata may also prey on holothurians and
226 S.:K: "WU
feeds on fragments of Turbo, the flesh
of which is made available by ophiuroids.
М. granulata was successfully kept
in the laboratory with Jsognomon and
Ostrea. The species exhibits 3
interesting characteristics: it shows a
preference for Ostrea rather than for
Isognomon; the species is gregarious
when feeding, and it has a tendency to
“prefer” feeding on deadorganisms when
both living and dead organisms are
available.
The proboscis performs a prominent
role in feeding. It first appears in
“searching” for the prey and “selects”
an acceptable drilling site. When fully
extended the proboscis is equal inlength
to the height of the shell. It is very
flexible and able to rotate in any di-
rection. Examination of shells on which
М. granulata had preyed indicated that
the snail drilled only the thinnest portion
of the shell of the prey.
The proboscis also plays a role in the
mechanical drilling of the shells of
Isognomon and Ostrea. Drilling involves
the radula, the musculature of the pro-
boscis, and the buccal mass, all of which
work together; it is alsocorrelated with
the presence of an accessory boring
organ (Carriker, 1961) or pedal gland
(Fretter, 1941) located in a sac, opening
into the sole of the foot near its anterior
end. It is concluded from behavioral
studies that the accessory boring organ
secretes a shell-softening substance
(Carriker, 1943, 1961). A detailed
account of drilling by muricids has been
given by Carriker (1943). In M. granu-
lata some rasping strokes were observed
but the detailed phases of drilling were
not observed.
Ciliary currents. Ciliary currents
were not apparent in the buccal cavity.
Those in the esophageal region (Pl. V,
Fig. 3), the stomach (Pl. V, Fig. 5),
the intestine and the rectum are similar
to those of D. ricina. The fecal pellets
which were obtained near the anus are
black, pointed at both ends and slightly
twisted. They are composed of fine
black granules (2 - 3 u in diameter),
various kinds of diatoms, filamentous
green algae and sponge spicules. The
feces are surrounded by a thin, trans-
parent film of mucus.
COMPARATIVE FUNCTIONAL
MORPHOLOGY OF THE DIGESTIVE
SYSTEM OF
D. RICINA AND M. GRANULATA
Although D, vicina and М. granulata
differ from one another in certain
features of their anatomy, the functional
morphology of the digestive system in
both species can be most fruitfully ex-
plored by way of a comparative dis-
cussion of the feeding habits, structure
and function of the digestive system of
the 2 species, and by a comparison of
those with previous descriptions of the
muricid digestive system.
D. vicina and M. granulata, living in
distinct ecological niches, also have
different feeding habits. Although the
feeding habits of D. vicina were not
observed, it is inferredfrom the associ-
ated plants and animals, the radula and
stomach contents, that D. ricina is
apparently not a boring gastropod but
probably feeds on carrion, deposits and
/or living sponges and holothurians. М.
granulata, on the other hand, was ob-
served to bore actively into bivalves
such as /sognomon and Ostrea, although
it preferred feeding on carrion even in
the presence of both living bivalves.
The buccal cavities of D. ricina and М.
gvanulata are similar to that of Urosal-
pinx cinerea (Carriker, 1943). The walls
of the buccal cavity are modified in
association with the movement of the
odontophore during feeding. The ventral
jaw, forming a concave surface which is
lubricated by the secretion of the salivary
gland, provides space against which the
odontophore slides back and forth, and
the lateral furrow of the wall can expand
allowing for the extrusion of the odonto-
phore.
The distinctive “drupid” and “morulid”
radular patterns displayed by each
species may possibly be associated with
the feeding habits of each species. In
D. vicina, where there are 5 cusps, of
which the laterals are clearly denticu-
lated medially and laterally and where the
a a OA
ae oe
FIG.
FIG.
FIG.
FIG.
FIG.
w №
DIGESTIVE SYSTEMS OF TWO MURICIDS 227
PLATE V
5
Drupa ricina; a portion of transverse section of the dorsal fold of the nerve-ring
portion of the mid-esophagus.
Morula granulata; a portion of transverse section of the rectal gland.
Drupa vicina; esophageal region, incised from the dorsal side at anterior half and
lateral side at posterior half of the figure, showing both internal surface and ciliary
currents (arrows).
Drupa ricina; the stomach, incised from the dorsal side, showing both structure and
ciliary currents(arrows).
Morula granulata; the stomach, incised from the dorsal side, showing both structure
and ciliary currents (arrows).
228 S. K. WU
rachidian base is not indented, the radula
is apparently a functional rasping organ.
In M. granulata where there are 3 smooth
cusps with a free denticle between the
central and the lateral cusps, 2 wrinkles
rather than denticles lateral to the lateral
cusps, and a rachidian base with an
indentation or pit in which sit all the
cusps, the radula functions in both boring
and rasping. Architecturally this kind
of a rachidian tooth would seem to have
great advantages in boring, the pit
forming a firm base for any boring
activity of the cusps.
In the formative portion of the radula
the lateral teeth overlap the rachidian,
forming a long, narrow band. The tips
of all the teeth point backward except
when the odontophore is protruded, at
which time the rachidian cusps are
oriented anteriorly and the tip of the
lateral teeth antero-laterally. In re-
traction the movement of the radula is
reversed and the teeth are again oriented
posteriorly. This motion makes it
possible for the central elevation of the
dorsal jaw to function as a surface which
aids in the removal of food and shell
particles from the radula.
In the organ of Leiblein, the almost
circular fold perhaps not only acts asa
valve, preventing the regurgitation of
food into the anterior-esophagus
(Graham, 1941) but might also create
a negative pressure by means of the
vibration of the long cilia which rim
the edges of the fold. The structure
responds to the forward thrust of the
proboscis during the feeding stroke.
The dorsal folds of the mid-esopha-
gus, developing after the organ of Leib-
lein in the region of the nerve-ring and
the convoluted portion, function in the
rejection of food particles. The dorsal
folds are rich in mucoid cells and in-
filtrated with phagocytes. The presence
of phagocytes among the mucoid cells
Suggests that the phagocytes may enter
the mid-esophagus at this point and that
some phagocytosis may occur inthis area
of the digestive tract. The dorsal folds
fade away immediately after curving into
the duct of the gland of Leiblein. The
wall of the dorsal groove of the mid-
esophagus is lined by simple cuboidal
cells, their structure suggesting that
no secretions are produced in the dorsal
groove.
The function of the salivary gland is
apparently that of lubrication. Although
the aperture of the duct of the salivary
gland has been described as opening into
the dorsal part of the cavity above the
tip of the odontophore in some muricids
(Graham, 1941; Carriker, 1943), in D,
ricina and M.granulata the duct descends
from the dorsal fold and opens into the
buccal cavity through the ventro-lateral
wall, near the lateral side of the ventral
jaw. Thus, the function of the salivary
gland apparently is associated with the
movement of the ventral jaw during the
outward and inward movement of the
odontophore in the feeding stroke, and
it is reasonable to assume that the
secretion is a lubricant. A proteolytic
enzyme was suggested by Mansour-Bek
(1934) to be secreted by the salivary
gland in Murex and by Mendel and
Bradley (1905) to occur in Busycon.
The function of the accessory salivary
glands in the muricids remains unknown.
As already described, there are 2 signifi-
cant differences in the accessory. sali-
vary glands of D, vicina and M. granu-
lata. The first difference relates to the
position of the accessory salivary gland
with respect to the salivary mass. InD,
vicina a pair ofaccessory salivary glands
is located ventro-laterally andfree from
the salivary gland. In M. granulata the
left accessory salivary gland is com-
pletely embedded in the salivary mass
while the right accessory salivary gland
remains free. The second difference
involves the accessory salivary glandit-
self. In D. ricinia there is a symmetri-
cally developed pair of accessory sali-
vary glands while in M. granulata the
pair of glands is not symmetrically
developed, the right accessory salivary
gland being smaller than the left one.
The asymmetrically developed ac-
cessory salivary gland in М. granulata,
DIGESTIVE SYSTEMS OF TWO MURICIDS
the absence of accessory salivary glands
in Murex pomum and their extremely
small size in Bedeva hanleyi, Murex
fulvescens, and M. fulvescens arenarius
(Carriker, 1961) deprecate the possible
role of these glands in the boring
process - as does the fact, reported by
Graham (1941), that the secretion of the
accessory salivary gland of Nucella
lapillus has a pH of 6 and does not etch
shell or dissolve shell flakes.
That the function of the accessory
salivary gland may be that of lubri-
cation, particulary associated with the
raking food habit, is suggested by the
position of the duct opening, and the
contrasting development nfthe accessory
salivary gland in D. ricina and M. granu-
lata.
The epithelial cells of the tubules of
the gland of Leiblein are club-shaped
cells as described by Graham (1941) for
Nucella lapillus. There are 2 types of
epithelial cells: mucoid and “granular”.
During secretion the round apical end is
nipped off. The secretion in the lumen
consists of granules, mucus and phago-
cytes. The secretionis moved away from
the lumen in a spiral string by the ventral
fold of the duct of the gland of Leiblein
to the posterior esophagus (Pl. V, Fig. 3).
It has been suggested that the secretion
of the gland of Leiblein probably contains
enzymes which split protein molecules
(Mansour-Bek, 1934).
The stomachs of D. ricina and M.
granulata differ externally. In D. ricina
the esophagus leads straight into the
center of the stomach which is a U-
shaped structure with a pouch at left
side of the esophageal opening. In M.
gvanulata the stomach is also U-shaped
but it does not possess this pouch. In-
ternally the stomach surface of both
species is identical, showing the
structural landmarks of the stomach of
a generalized prosobranch, as described
by Graham (1949).
The stomach is also to be interpreted
in the light of the particular feeding
habits of the 2 species. In D. ста the
pouch at the base of the U is remi-
229
niscent of some ofthe omnivorous meso-
gastropods and of a style-bearing steno-
glossan neogastropod, Cyclope neritea,
which is both a carrion and deposit
feeder (Morton, 1960). In M. granulata.
the typical U-sac is reminiscent of the
stomach of Trivia (Mesogastropoda)
which feeds on ascidian zooids (Fretter,
1951) and of Murex, which is typically
an active predator (Carriker, 1961).
The function of the stomach in both
Species is that of mechanically rotating
and moulding the food bolus. A sorting
mechanism such as was described for
some of the carnivorous mesogastropods
(Graham, 1949) was not observed. Parti-
cles in the intestinal groove were not
observed to enter either aperture of the
digestive gland, but to be drawn out,
all particles being rejected by ciliary
currents.
The digestive gland is mainly
composed of “digestive” cells but at the
terminal end of each tubule there are
also grouped “secretory” cells (Fretter
& Graham, 1962). The “digestive” cells
are filled with granules which stain
variously, indicating that a number of
complicated chemical changes occur
within these cells. The function of
these cells, whether absorptive or se-
cretory, has not been determined. How-
ever, the rejection of particles by the
intestinal groove, and the club-shaped
apical end of the “digestive” cells suggest
that secretion is probably the principal
activity of the digestive gland. The
“secretory” cells, with their triangular
bases facing the visceral hemocoel, may
take up materials from the blood and
elaborate these materials into some
secretion which is then shed into the
lumen of the tubule (Fretter & Graham,
1962).
The intestine of р. ricinaandM. granu-
lata differs slightly in the development
of the epithelial folds, those of D, уста
being more developed than those in M.
gvanulata. The surface of the intestinal
epithelium of M. granulata is smooth,
interrupted on occasion by notches. The
more folded intestine of D, vicina offering
230 S. K. WU
a greater surface, might perhaps be
associated with an omnivorous diet. The
notches in the epithelium in M. granulata
might permit the infiltration of phago-
cytes from surrounding tissues.
The rectum shows considerable longi-
tudinal folding and again there are a
large number of phagocytes in the lumen
of both species. The rectum is sur-
rounded by blood spaces. The presence
of phagocytes again suggests a site
where absorption occurs. In addition, the
rectum dehydrates the feces, which
becomes more solid towards the anal
end, and also molds it.
The occurrence of large numbers of
undigested diatoms and algae in the
feces indicates that no enzymes are
present which can digest these sub-
stances.
The rectal glands of D. vicina and
M. granulata are significantly different:
in the latter species it is black and is
easily distinguishable externally, while
in the former it is light yellow and has
an obscure outline. The function of the
rectal gland, according to Fretter (1946)
is that of abstracting excretory matter
from the blood. A well-developed rectal
gland thus would be advantageous to
carnivorous snails whose food contains
much nitrogeneous material.
DISCUSSION
The muricid genera Drupa and Morula
have long been considered closely re-
lated conchologically, and in fact are
separated only on the basis of size
(Morula including the smaller, ovate
species), sculpture (Drupa with spines
and Morula with nodules), shape (Drupa
with a low spire and Morula with a high
spire) and the teeth of the outer lip
(Drupa with grouped teeth and Morula
with single teeth). Cooke (1919) pointed
out that the radulae of the 2 genera are
distinct.
The results of the comparative studies
of the digestive system of one species
in each genus also indicate that Drupa
and Morula are deserving of generic
separation. The 2 species representing
the genera not only live in distinct
ecological niches, but also apparently
have different feedinghabits. Correlated
with their feeding habits are the
structural differences in the digestive
system described above.
The Muricacea, although well known
for their predatory habits, have recently
been considered to be the most primitive
of the stenoglossan gastropods (Fretter
& Graham, 1962). From the point of
view of the digestive system the Steno-
glossa as a suborder are characterized,
in general, by a narrow band of radula,
a long pleurembolic type of proboscis,
the gland of Leiblein, frequently a simpli-
fied stomach, a short intestine and
sometimes, a rectal gland.
In the Muricacea the organ of Leiblein
is well developed and the effects of
torsion are apparent anterior to the
nerve-ring. The dorsal fold can be
traced throughout the length of the
esophagus. The gland of Leiblein is
bulky. The accessory salivary gland,
the accessory boring organ and the
rectal gland are present.
These features are to be contrasted
with those of the other 2 superfamilies
of the Stenoglossa, the Buccinacea and
the Volutacea where the organ of Leib-
lein is not well developed, and the
effects of torsion are apparent posterior
to the nerve-ring. The dorsal folds
of the mid-esophagus are less obvious.
The gland of Leiblein is less developed,
and both the accessory salivary glandand
the accessory boring organ are lacking.
Within the Muricacea, assuming the D,
vicina and М. granulata are representa-
tive species of their respective genera,
both Drupa and Morula exhibit clearly
primitive features from the standpoint
of the evolution of gastropod feeding
habits and stomach structure. The
primitive features of Drupa and Morula
are not reflected inthe proboscis, radula,
or esophagus, all of which show striking
similarities to those which have been
previously described for muricids
(Carriker, 1943; Graham, 1941), but in
DIGESTIVE SYSTEMS OF TWO MURICIDS 231
the stomach pattern. The stomach of
both D. ricina and M. granulata differs
significantly from the simplified stomach
of Nucella lapillus described by Graham
(1949) in that it still shows a definite
style sac region, “gastric shield” region,
and, on occasion, a protostyle. The
difference between Drupa and Morula on
the one hand and Nucella on the other
is further emphasized by the presence of
2 apertures of the digestive gland in
the former 2 species, contrasting with the
Single aperture described by Graham
(1949) in Nucella. Two apertures of
the digestive gland, however, have been
described for Murex erinaceus (Sim-
roth, 1896-1907), a higher carnivorous
form.
The stomach patterns of both р. vicina
and M. granulata closely resemble that
of Trivia (Graham, 1949), a carnivorous
member of the Mesogastropoda, the sub-
order from which the Stenoglossa are
currently thought to have originated.
Among the Stenoglossa, the stomach
patterns of D. ricina and М. granulata
resemble most closely that of the nas-
sariid, Cyclope neritea, a member of
the Buccinacea (Morton, 1960). Morton
has pointed out that the style sac, gastric
Shield, and protostyle of this species
are evidence for its primitive status
within the Buccinacea, and he suggested
that deposit feeding and primitive
stomach patterns, which are generally
characteristic of the Prosobranchia, may
be retained among the lower members of
the generally more advanced Steno-
glossa. The feeding habits and stomach
patterns of Drupa and Morula may thus
be interpreted as representing the basal
or primitive features of the Stenoglossa,
reflecting their mesogastropod an-
cestry.
ACKNOWLEDGMENTS
This work was carried out in the
Department of Zoology, University of
Hawaii under the guidance of Dr. E. A.
Kay, to whom I am very grateful for
stimulating and fostering my interest in
the Muricacea. Thanks are also grate-
fully extended to Dr. D. C. Matthews of
the University of Hawaii for his advice
and attention regarding the manuscript;
to Dr. Yoshio Kondo, Department of
Mollusks, Bernice P. Bishop Museum,
Honolulu, for allowing and encouraging
me to study the museum specimens;
and to Dr. M. R. Carriker, Marine
Biological Laboratory, Woods Hole and
Dr. K. Y. Arakawa, Miyajima Aquarium,
Hiroshima, Japan who have taken time
to answer my questions.
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GRAHAM, A., 1939, On the structure
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, 1941, The oesophagus of the
stenoglossan Prosobranchs. Proc.
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, 1949, The molluscan stomach.
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761:
, 1955, Molluscan diets. Proc.
malac. Soc. London, 31: 144-157.
HALLER, B., 1888, Die Morphologie
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HERRICK, J. C., 1906, Mechanism of
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707-737.
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HIRSCH, G. C., 1924, Der Weg des
resorbierten Eisens und des phago-
cytierten Carmins bei Murex trun-
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KAY, A., 1960, The functional mor-
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and an interpretation of the relation-
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KEEN, A. M., 1958, Sea shells of
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MANSOUR-BEK, J. J., 1934, Uber die
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MENDEL, L. B. and BRADLEY, H. C.,
1905, Experimental studies in the
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Physiol., 13: 17-29 (vide GRAHAM,
1941).
MILLOT, N., 1937, On the morphology
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feeding and physiology of digestion of
the nudibranchiate mollusc, Jorunna
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Soc. B., 228: 173-217.
MORTON, J. E., 1952, The role of the
crystalline style. Proc. malac. Soc.
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, 1953, The function of the
gastropod stomach. Proc. Linn. Soc.
London, 164: 240-246.
, 1955a, The functional mor-
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(Gastropoda Pulmonata) with special
reference to the digestive and repro-
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Soc. London, B., 239: 89-160.
, 1955b, The structure and
function of the stomach and sorting
DIGESTIVE SYSTEMS OF TWO MURICIDS
caecum in Lunella samraga (Martyn)
(Turbinidae). Proc. malac. Soc.
London, 31: 123-137.
‚ 1960, The habits of Cyclope
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gastropod. Proc. malac. Soc. London,
34: 96-105.
NAKAJIMA, M., 1956, On the structure
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of the feeding habits and systematic
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115.
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Soc. London, 33: 103-114. -
RISBEC, J., 1955, Consideration sur
l’anatomie comparée et la classi-
fication des gasteropodes proso-
233
branches. J. Conchyl., 95: 45-82.
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TAYLOR, D. W. and SOHL, N. F., 1962,
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Biologicae, 2: 1-19.
‚1961, Thecomparative physi-
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WHITAKER, M. B., 1951, Onthehomol-
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malac. Soc. London, 29: 21-34.
RESUMEN
y SISTEMA DIGESTIVO DE DOS MURICIDOS
En las Islas Hawaii Drupa ricina (L.) habita un lujuriante ambiente algológico, con
holoturias y esponjas. Morula granulata (Duclos) vive en áreas con menor desarrollo
de algas, junto con el bivalvo Isognomon y esponjas.
La anatomía e histología del aparato digestivo de D. ricina se describe en detalle y
en comparación con M. granulata. En general son similares, excepto en sus rádulas,
complejo glándular, estómago y glándulas rectales. D. ricina tiene dientes raquídeos
con 5 cúspides sin base hueca, mientras que M. granulata tiene 3 cúspides y base
hueca. Dos diferencias significativas se asocian con el complejo glandular: en D,
ricina un par de glándulas salivares accesorias estan desarrolladas simetricamente
y separadas de la masa glandular salivar, y en M. granulata la glándula accesoria
izquierda, más grande, esta completamente incluída en la masa, y la derecha que es.
más pequeña, permanece libre. EI estómago difiere externalmente: en ambas es
como un saco en forma de U pero en D. ricina tiene una bolsa sobre el lado faríngeo,
que falta en М. granulata. La glándula rectal en D. ricina es amarillo-clara y de con-
tornos no definidos, mientras en M. granulata es negra y bien distinguible externa-
mente.
Se discuten los aspectos funcionales del sistema. Cavidad bucal, glándulas sali-
vares y sus accesorias estan relacionadas con la lubricación durante la alimentación.
Corrientes ciliares existen en el sistema entero, excepto en la cavidad bucal.
Se observó que Morula taladra los bivalvos, aunque prefiere carnes muertas,
mientras que Drupa no parece ser un enemigotipico de los moluscos con concha dura,
sino que subsiste sobre una variedad de presas eomo holoturias y esponjas. Los
hábitos alimenticios y diferencias dietarias se ubican en relación a las diferencias es-
tructurales; comparación de estos aspectos y de los estómagos de Drupa y Morula con
la de los Mesogastropodos carnívoros y otros Estenoglosos, pueden indicar que ambos
géneros representan las caracteristicas primitivas de los Estenoglosos, reflejando
su ascendencia mesogastropoda.
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MALACOLOGIA, 1965, 3(2): 235-262
MARINE EUTHYNEURAN GASTROPODA FROM ENIWETOK ATOLL,
WESTERN PACIFIC]
Ernst Marcus2 and J. В. Burch?
ABSTRACT
This study is based on a collection of marine euthyneuran mollusks made by
the second author at Eniwetok Atoll, Marshall Islands, during February-April,
1960. Seventeen species were collected, of which 5 are described in this paper
as new species. The new species are: Haminoea musetta, H. linda, Chromo-
doris briqua, Herviella mietta and Onchidella evelinae. Of the other 12 species,
the distribution of 7 of them extends eastward from the western Indian Ocean (2
also occur in the Red Sea) to Eniwetok or farther east; 2 species are circum-
tropical or circumsubtropical; 2 species are known only from the western
Pacific; and 1 species occurs from Eniwetok westwards into the eastern Indian
Ocean. The relative uniformity of the western Indopacific reef fauna is indicated
by the fact that 9 (or over 50%) of our species are known to range from the
western edge of the Indian Ocean to the western or central Pacific. The genus
Herviella seems to be confined to the western Pacific. Thenotogaeic occurrence
of an Onchidella with a ventral recurrent limb of the kidney and a cuticular
stylet in the diverticulum of the penial pouch is remarkable.
Eniwetok Atoll comprises a group of
some 30-odd coral islands inthe western
Pacific. Eniwetok is one of several such
atolls which make up the Marshall Islands
of Micronesia. During the months of
February-April, 1960, the second author
and Dr. William H. Heard collected
mollusks on 4 islands of Eniwetok Atoll.
The present report is based on the 17
species of euthyneuran gastropods col-
lected at that time. All specimens,
except representative series sent to the
University of Hawaii and the University
of Säo Paulo, are now in the collections
of the Museum of Zoology, University
of Michigan.
Grateful acknowledgement is made to
the United States Atomic Energy
Commission for supporting the study of
the second author at Eniwetok by pro-
viding travel funds, logistical support and
use of the facilities of the Eniwetok
Marine Biological Laboratory. The
cooperation of the U.S. A. E. С. Eniwetok
Field Office, Task Group 7.1, and Holmes
and Narver, Inc., greatly facilitated the
field collecting. A note of gratitude is
due to Dr. I. Eugene Wallen, U.S.A.E.C.,
Dr. Robert W. Hiatt, University of
Hawaii, and Prof. Henry van der Schalie,
University of Michigan, for promoting
these studies, and to Dr. William H.
Heard, Florida State University, for
assistance while at Eniwetok. Acknow-
ledgement is also due Mrs. Eveline du
Bois-Reymond Marcus for assistance to
the senior author and for preparing the
illustrations.
MATERIALS AND METHODS
The animals reported on here were
lThe field work for this investigation was supported by the Division of Biology and Medicine,
U. S. Atomic Energy Commission.
2University of Säo Paulo, Brazil.
3Museum and Department of Zoology, University of Michigan, Ann Arbor, Michigan, U. S. A.
Supported (in part) by a Public Health Service research career program award (number
5 K3-AI-19, 451) and by research grant 5 T1 AI 41-07 from the National Institute of Allergy and
Infectious Diseases, U. S. Public Health Service.
| (235)
236 MARCUS AND BURCH
collected from various localities on 4
islands of Eniwetok Atoll: "Eniwetok I.,
Parry I., Japtan I. and Annaianni I.
Most of the specimens were anesthetized
before being fixed and preserved. A
number of different anesthetizing re-
agents were used: chlorotone, chloral
hydrate, menthol, magnesium chloride,
nembutal and propylene phenoxetol.
Three different fluids were used for
fixing the specimens: Bouin’s fluid, AFA
(alcohol-formalin-acetic acid) and 10%
neutralized formalin. The animals were
preserved in either 5% formalin, 1%
propylene phenoxetol or 70% ethanol.
The most satisfactory technique for
preserving nudibranchs was a modifi-
cation of the method of Hanna (1955). The
living animals were frozen in sea water
in a freezer; the ice was then melted
with 10% formalin and the animals were
transferred to 1% propylene phenoxetol.
Sketches and color photographs were
made of the living animals, accompanied
by notes of external characters, colors,
measurements, etc.
SYSTEMATICS AND DISTRIBUTION
A systematic list of species of Euthy-
neura collected at Eniwetok during the
field study are listed below. The species
are treated individually in consecutive
order in the section following the list.
Cephalaspidea, Philinacea, Smaragdi-
nellidae
1. Smaragdinella calyculata (Brod-
erip and Sowerby, 1829)
2. Lathophthalmus smaragdinus
(Rüppell and F. S. Leuckart,
1828)
Cephalaspidea, Bullacea, Atyidae
3. Haminoea musetta, new species
4, Haminoea linda, new species
9. Lamprohaminoea cymbalum
(Quoy and Gaimard, 1833)
Anaspidea, Aplysiidae, Dolabriferinae
6. Dolabrifera dolabrifera (Rang,
1828)
Anaspidea, Aplysiidae, Notarchinae
7. Stylocheilus longicauda (Quoy and
Gaimard, 1824)
Doridoidea, Eudoridacea, Crypto-
branchia, Dorididae, Chromodoridinae
8. Chromodoris fidelis (Kelaart,
1859)
9. Chromodoris briqua, new species
10. Hypselodoris hilaris (Bergh,
1890)
Doridoidea, Eudoridacea, Phanero-
branchia, Nonsuctoria, Gymnodorid-
idae
11. Gymnodoris bicolor (Alder and
Hancock, 1864)
Doridoidea, Porostomata, Dendro-
dorididae
12. Dendrodoris nigra (Stimpson,
1855)
13. Dendrodoris erubescens (Bergh,
1905)
Eolidoidea, Cleioprocta, Favorinidae,
Favorininae
14, Herviella claror Burn, 1963
15. Herviella mietta, new species
Soleolifera, Onchidiacea, Onchidiidae
16. Onchidella evelinae, new species
Basommatophora, Siphonariacea,
Siphonariidae
17; Siphonaria (Sacculosiphonaria)
guamensis (Quoy and Gaimard,
1833)
1. Smaragdinella calyculata (Broderip
and Sowerby, 1829)
(Figs. 1-5)
Pilsbry, 1895, p 258 (viridis), pl. 33,
figs. 42, 45-53 (viridis and glauca);
Bergh, 1901, p 228, pl. 19, figs. 39-45
(viridis); Habe, 1952, p 144, 146, pl. 20,
fig. 07e pls 2194122726:
Occurrence: In lagoon at north end of
Eniwetok Island.
Further distribution: Southern Indian
Ocean, Reunion and Mauritius; Java
(Adam and Leloup, 1938, p 199); middle
Japan, Seven Islands off Izu; southern
Japan, ShikokuIsland, Amami and Ryukyu
Groups; Mariana Islands, Guam;
Hawaiian Islands; Pitcairn Island;
PACIFIC EUTHYNEURA 237
FIGS. 1-5. Smaragdinella calyculata. Fig.
Fig. 5. Male genital structures; A, atrium;
Hancock’s organ;
. Living animal dorsal view, drawn from Kodachrome
transparency. Fig. 2. Right side viewof anterior part. Fig. 3. Inner side of shell. Fig. 4. Radular teeth.
CS, cephalic shield; E, eye; GO, genital opening; HaO,
M, mouth; MD, male duct; MV, muscular vesicle; Pa, parapodia; PM, posterior
mantle lobe; Pr, prostate; RMu, retractor muscle; SG, seminal groove; Sh, shell; SV, seminal vesicle.
Easter Island (Odhner, 1921), p 248;
not Dall, 1908, as Odhner’s asterisk
indicates).
The shell is mainly external, solid,
the one measured was 6 mm long, 3.8
mm broad. The shell’s apexis concealed.
The outer lip of the aperture is angular
posteriorly without a thickening in the
Shell examined. The columellar border
runs out into a cup-shaped process pro-
jecting forward into the aperture. In
living animals the shell is diaphanous
yellow; inpreserved animals itis opaque
white, green on the inner side and witha
transparent periostracum.
A large snail was 14 mm long and 8.5
mm broad when crawling; 4 preserved
Specimens measured 11, 9.5, 7.5 and 6
mm in length. The body in life is pale
green with many opaque white spots and
a somewhat smaller number of scattered
small black spots. White spots occur in
patches along the colorless edge of the
foot and on the posterior lobe of the
mantle. White marks occur onthe para-
podia and also on the cephalic shield,
where they are less numerous. The
small black eyes (Fig. 1, E) are situated
farther from the mid-line than from the
sides. There is an opaque white oval
area at the hind end of the cephalic
shield (CS), followed by many rather
uniformly spaced black spots which show
through the shell (Sh). These spots are
larger than the ones previously men-
tioned. Farther backward growth lines
of the shell can be seen between the
parapodia (Pa).
The cephalic shield is nearly straight
in front. In living animals it extends
to the middle of the body and ends with a
blunt point. In preserved specimens
238 MARCUS AND BURCH
the posterior terminus of the cephalic
shield is slightly bilobed and located
near the anterior border of the shell.
Hancock’s organ has only dorsal pinnae
and it lies under the cephalic shield,
dorsal to the seminal groove (Fig. 2,
SG). The end of the foot does not ex-
tend beyond the visceral hump.
The jaw elements are rod-shaped. The
radula (Fig. 4) is light yellow, consisting
of 30 rows with 19, rarely 20, teeth per
half-row. The rhachidian plate is 47
micra high, more slender than in Habe’s
(1952) figure (pl. 21, fig. 26), with a
central cusp, but without lateral
denticles, so that it agrees with Habe’s
figure and differs from Bergh’s (1901)
S. glauca (p 240, pl. 19, figs. 47, 48).
The lateral plates have long, hook-shaped
cusps. The 5-6 outermost lateral plates
lack cusps. The cusp of the innermost
lateral tooth measured 57 micra in
length; the cusp of the next lateral tooth
measured 65 micra. The length of the
cusps increased to 72 micra in the
middle of the row and decreased out-
ward. The bases of the 8 outer teeth
are broad; the bases of the 5-6 inner
ones have basal striae, as also occur
in several species of Haminoea. The
gizzard plates are conchinous, black
in front, ivory behind, with a median
crest and many ridges on either side.
The common genital opening (Fig. 2,
GO) is located far in front, in front of
the posterior end of the cephalic shield
(CS). The seminal groove (SG) is
straight, its aperture at the level of the
anterior end of Hancock’s organ (HaO) as
in Haminoea. The male atrium (Fig. 5,
A) is wide, with a folded epithelium and
a muscular wall. The male duct (MD)
has a terminal seminal vesicle (SV), a
bilobed prostate (Pr), and a second
muscular vesicle (MV). One bundle of
the retractor muscle (RMu) inserts on
this vesicle; some fibers insert on the
loop of the male duct and on its straight
section between loop and atrium.
Discussion of Smaragdinella calyculata
Pilsbry (1895, p 259) and Pruvot-Fol
(1934, р 24) consider $. viridis, now
known as 5. calyculata, and S. glauca,
whose type-specimens are lost, as one
and the same species. If thisis correct,
the shape of the inner process of the
Shell, like a lancet in Zilch’s specimen
(1959, fig. 144), like a cup in Risbec’s
material from New Caledonia (1951, fig.
VII, 3), is systematically insignificant.
In fact, shells such as those drawn by
Pilsbry (1893-95, pl. 33, fig. 47), Thiele,
(1931, fig. 487), and Habe (1952, fig. 7)
are intergrades between the mentioned
extremes. Bergh’s diagnoses of S,
viridis and S. glauca, whichhe separates,
do not reveal palpable differences; his
description of the male organ is in-
complete. Risbec’s figure of the living
animal (pl. 8, fig. 9) hardly represents
a Smaragdinella. In his anatomical
record only the size of the lateral gizzard
plates is a little smaller than the central
one, and the shape ofthe latter disagrees
with what is known of $. calyculata. If
Risbec’s animal is another species, it
must be renamed; he published it as
Smaragdinella viridis, n. sp.
2. Lathophthalmus smaragdinus (Riippel
and F. S. Leuckart, 1828)
Marcus, 1960a, p 884-890, figs. 14-21
(bibliography and description).
Occurrence: Very abundant at Eni-
wetok Atoll during March, 1960. Col-
lected at the south end of Parry Island,
under stones on seaward tide flat; March
15, 1960.
Further distribution: Indo-West Pa-
cific Ocean, from the Red Sea to southern
Ryukyu and Fiji Islands.
The living animals measure up to 35
mm in length when extended. Two pre-
served specimens measured 19 x 8.5
and 16 x 7 mm. Correspondingly, their
cephalic shields were 6 x 5 and 3.8 x 3
mm. The Hancock's organ had 15 leaves
in the larger of the 2 animals, and 20
leaves in the smaller one. The position
of the eyes in relation to the Hancock's
organ is the same in both specimens.
The mantle foramen which leaves part of
the shell free is the best distinguishing
PACIFIC EUTHYNEURA 239
FIGS. 6-11. Haminoea musetta, n. Sp.
Fig. 10. Diagram of male genital structures.
Fig. 6. Living snail, drawn from Kodachrome transparency
dorsal view. Fig. 7. Radula, central and first lateral teeth. Fig. 8. Right Hancock’s organ. Fig. 9. Shell.
Fig. 11. Detail of penial papilla; A, atrium; AS, atrial
sheath; CS, cephalic shield; E, eye; Fu, fundus of atrium; Ma, mantle under shell; MP, male duct;
Pa, parapodia; PM, posterior mantle lobe; Pr, prostate; RMu, retractor muscle; SG, seminal groove;
SV, seminal vesicle.
character of Lathophthalmus, Pruvot-
Fol, 1931 (p 748) separating it from
Phanerophthalmus A. Adams, 1850; but
the distinction is not easy (Pruvot-Fol,
1934, p 30).
3. Haminoea musetta, new species
(Figs. 6-11)
Occurrence: North (collection A) and
middle (collection B) parts of Parry
Island on seaward tide flats; March 25
and April 2, 1960.
Shells (collection A): 8-9 mm high,
5-6 mm wide; greatest breadth about
in the middle of the shell or slightly
anterior of the middle; (collection B):
6.5-7.2 x 4.3-5.5 mm, greatest breadth
in the middle of the shell. Ratios of dia-
meter to height are 1:1.31 to 1:1.50. Shell
shape (Fig. 9) swollen, ovoid. Shell
with 11/2 whorls, rather fragile, shining,
slightly narrowed posteriorly. The axial
growth lines are more or less distinct;
the spiral striae are extremely fine.
The outer lip of the shell is convex and
well-curved. It covers the apex slightly,
rising to the right of the sunken spire.
The apex may have a small perforation
(collection A) or it may be imperforate
(collection B). The columella is deeply
concave, its base reflected. The colu-
mellar callus is separated from the body
whorl by a furrow; its enamel layer
extends farther posteriorly in the
smallest shell of collection A than inthe
largest one of collection B.
Living snails measure up to 15 mm
when crawling (Fig. 6); a preserved
extended animal of collection A measured
11 mm; specimens of collection B were
all retracted into their shells. Colors
in life (collection A): ground color
very pale green; mantle (Ma) speckled
with dark green and black spots, and
green ones with black centers, and a
few blank areas without pigment showing
240 MARCUS AND BURCH
through the shell. On the cephalic
shield (CS) and the parapodia (Pa) the
spots are confluent, producing a mottled
aspect. In collection B the green spots
are less numerous, and the cephalic
shield and parapodia are spotted like the
rest of the animal, not mottled as on the
specimens of collection A. White spots
occur everywhere on the animals in
clusters, which show through the shell.
There are also a number ofbrown spots,
except under the center of the dorsal
part of the shell.
The cephalic shield is slightly notched
in front, with two long flaps behind; the
parapodia in living specimens reachhalf
the length of the shell; in preserved
snails (collection A) they are relatively
longer. Hancock’s organ (Fig. 8) is
pinnate, the dorsal pinnae being longer
than the ventral ones. The ends of the
dorsal pinnae are often covered by a fold.
The jaws are semicircular with pris-
matic rodlets which are about 50-100
mi¢cra high: "and 10x 18: паста. in
diameter. The radula contains 25-35
rows of teeth with 9-10 laterals per
half-row. The rhachidian tooth (Fig. 7)
is smooth with a rough base and strong
median and short lateral cusps. The
lateral teeth are all without denticles;
the cusps are longest in the middle of
each half-row. The gizzard plates are
brown with 17 smooth ridges.
Like in all Haminoeas, the male
aperture is at the anterior end of the
right Hancock’s organ, where the
cutaneous seminal groove (Fig. 10, SG)
enters the male atrium(A). Inthe present
species the latter is a long, muscular
tube within a thin sheath (AS). The
fundus of the atrium (Fu) has 2 pointed
epithelial, not cuticularized, lobes (Fig.
11). The male duct (MP) begins with a
small vesicle, then continues as a narrow
and winding tube without any spines.
The penial retractor muscle (RMu)
inserts near the middle of the male duct.
The succeeding coils of the duct leadinto
a slightly lobed, nearly globular, pros-
trate gland (Pr). The walls of the
prostate are glandular; its lumen (SV)
frequently (collection B) contains sperm
masses. There is no separate seminal
vesicle. The female organs are system-
atically insignificant.
The name of this species is derived
from “musette” = cornemuse, bagpipe.
Discussion of Haminoea musetta
The slight differences between the
shells and the colors of the soft parts
of collection A and B are taxonomically
insignificant, because the labial arm-
ature, the radula, andthe male copulatory
organs of the 2 collections are similar.
In classifying the Haminoea of the
present collection we went through the
same difficulties as Pilsbry (1921, p 368)
and Macnae (1962, p 187). The shell of
H. musetta is similar to that of the type
species of Haloa, H.crocata Pease,
(1860a, b, p 19, 432). Pilsbry (1921,
p 367) introduced Haloa as a section of
Haminoea; Zilch (1959, p 42) called ita
Subgenus; and Habe (1952, p 148) con-
sidered it as a genus. Habe indicated
that the first lateral tooth in Haloa had
2 cusps (actually an inner denticle in
addition to the cusp). Since Habe (p 150)
considered Vitrohaminoea, without such
denticle, as a subgenus of Haloa, the
denticle cannot be a generic character.
Therefore, we have to compare dH,
musetta with other Indo-West Pacific
Species without giving any consideration
to the radula.
The species with a shell most similar
to Haminoea musetta is that of H. nigro-
punctata Pease, 1868 (Pilsbry, 1895, p
365), but its soft parts differ by the longer
and more pointed flaps of the cephalic
Shield and the “rather posterior” para-
podia. Only black pigment spots were
described for H. nigropunctata. Hi
binotata Pilsbry, 1895 (1896, р 231)
has a much less developed callus (Habe,
1952, pl. 21, fig. 30) than H. musetta
and, in addition, peculiar color marks
on the shell. In its variety H. b. japonica
Pilsbry, 1895 (1896, p 232), today given
specific rank (Habe, 1961, p 11), the
columellar callus is adnate to the body
whorl. This character does not agree
therefore
PACIFIC EUTHYNEURA 241
with the original diagnosis of Haloa.
Pilsbry’s (1895, p 363, pl. 40, fig. 3)
first specimen of Haminoea crocata had
a “moderately concave” columella.
Later (1921, p 367, text fig. 6) he
described and figured a deeply concave
columella, such as occurs in A. musetta.
The outer lip rising at the apex is shown
in both of Pilsbry’s figures, and it is
described indirectly in his text. This
elevation of the outer lip distinguishes
Н. crocata and also H. callosa Preston,
1908 (p 189) from H. musetta. More-
over, the base ofthe columella is straight
in the figure of H. callosa (pl. 15, fig.
31). Probably Pease’s description ofthe
body color of H. crocata as “cinereous,
pellucid” and hence without any Spots,
is not systematically significant, because
Pease described preserved material, and
the pigment spots of Haminoea fade out
in the preserving liquids in contrast to
those of several other opisthobranchs.
In any case, the dark green color “with
large orange hieroglyphs” and the
characteristic shape of the foot of speci-
mens that Ostergaard called Н. crocata
(1955, p 112) showthat it actually belongs
tó H. simillima Pease, 1868 (Pilsbry,
1895, p 366; Eliot, 1906b, p 310).
The shell of Haminoea galba Pease
(1860 a, b, p 20, 432) is considered to
be hardly distinguishable from that of H.
crocata. It is, however, “perceptibly
less swolien” (Pilsbry, 1921, p 368) and
different from that of A.
musetta. The columella of H. galba
bears a fold in Sowerby’s figure (1868,
fig. 23), reproduced by Pilsbry (1895,
pl. 40, fig. 1); in H. musetta the
columella has no fold.
The epithelial lobes in the fundus of
the male atrium of H. musetta which
correspond to a penial papilla, “glans”
(Bergh) or “mamelon” (Guiart, 1901,
p 145) may be compared with some
earlier descriptions, namely those of
Bergh (1900, p 162; 1901, p 227, 229,
233), Si (1931, p 56), and Marcus (1958b,
p 37; 1961, p 6).
4. Haminoea linda, new species
(Figs. 12-16)
Occurrence: Parry Island, in sand,
in about 2 m depth, in lagoon, about 17
m from shore; March 31, 1960.
Shell 10 mm high, 7.5 mm wide;
greatest breadth in the middle. The
ratio of the shell diameter to the shell
height is 1:1.33. The shell (Fig. 14)
is swollen, ovoid, with 1 1/2 whorls,
very fragile, whitish, slightly shining,
narrowed anteriorly and posteriorly.
Under a magnifying lens fine growth lines
can be seen, but no spiral striae. The
outer lip is a little convex, covering the
minutely perforate apex. The columella
is deeply concave, its base reflected but
adnate to the body whorl. The very low,
broad callus extends to the apex.
The length of a measured crawling
snail was about 17 mm; one of the
larger preserved animals measured 11
mm in length. The ground color of the
animal is pale green with small orange
and maroon spots. Onthe cephalic shield
and parapodia the larger orange spots
are bordered with white. Very large
white spots with orange centers occur
under the shell. Confluent white patches
occur on the tail. The foot is spotted
much the same way as the cephalic shield
and parapodia. The various pigment
spots are of rather diverse size and
density.
The cephalic shield of Haminoea linda
is slightly notched in front, bilobed be-
hind. The parapodia cover somewhat
less than one-half the length ofthe shell.
Hancock’s organ (Fig. 15) is only a
simple ridge, hence different from that
known in other species of Haminoea
(Guiart, 1901, p 104-105; Hoffmann,
1935, p 608). '
The jaws are weak, their rodlets soft,
and measure 4-5 micra in diameter.
The radula contains about 25 rows, each
row with 8 teeth per half-row. The
rhachidian tooth (Fig. 13) is tripartite
242 MARCUS AND BURCH
FIGS. 12-16. Haminoea linda, n. sp. FIGS. 17-20. Lamprohaminoea cymbalum. Fig. 12. Living snail
of Н. linda, drawn from Kodachrome transparency, dorsal view. Fig. 13. Radula, central, 1st and 2nd
lateral teeth. Fig. 14. Shell. Fig. 15. Right Hancock’s organ. Fig. 16A. Diagram of male genital struc-
tures. B. Detail of penis. Fig. 17. Right Hancock’s organ of L. cymbalum, Fig. 18. Radula, central and
lst lateral teeth. Fig. 19. Diagram of male copulatory organ; 1 mm of atrium omitted. Fig. 20. Detail of
penis; A, atrium; AS, atrial sheath; CS, cephalic shield; E, eye; Fu, fundus of atrium; MD, male duct;
Pa, parapodia; Pe, penis; PM, posterior mantle lobe; Pr, prostate; RMu, retractor muscle; Sh, shell;
SV, seminal vesicle.
PACIFIC EUTHYNEURA 243
in front, its base is roughened, and its
median cusp has lateral denticles. The
lateral cusps of the rhachidian tooth are
broad, blunt, smaller than the median
cusp. The first lateral tooth has about
5 denticles on its inner side, which is
quite uncommon in Haminoea. The
remaining lateral teeth resemble those
found in other species of the genus. The
gizzard plates are greenish-brown with
17 smooth ridges.
The male atrium (Fig. 16A) in
Haminoea linda is a long muscular tube
(A) with a thin sheath (AS). The seminal
groove becomes a narrow Closed tube at
the fundus of the atrium. The duct
forms a short, conical dilatation with
6 cuticular spines at the entrance into
this dilatation and 9 longer ones at its
fundus (Fig. 16B (Fu)). Farther inward
the duct (MD) continues as anarrowtube
for a short way, then becomes embedded
in fibers of the penial retractor muscle
(RMu) and bends again toward the fundus
of the atrium. Some fibers of the penial
retractor muscle connect the duct and
the atrium. The duct is also surrounded
by the penial retractor muscle in its
Succeeding inward course, emerging
from the muscle near its middle. The
following free section of the duct is
lined by a high, vacuolated epithelium.
The duct opens into an acinous, nearly
globose prostate gland (Pr), which is
united entally with a clustery seminal
vesicle (SV).
The name of this species is the female
form of “lindo” = pretty (Portuguese).
Discussion of Haminoea linda
The color pattern of the new species
is similar to that of Haminoea ovalis
Pease, 1868 (Pilsbry, 1895, p 365, pl.
40, fig. 94; pl. 43, figs. 9-10, 17), and
H. aperta Pease, 1868. However, the
Shell of H. ovalis is shorter, and that
of H.aperta is longer. The shells of
H. vitrea (A. Adams, 1850) (see Pilsbry,
1895, pl. 40, fig. 83) and of H.rotundata
(Pilsbry, 1895, pl. 41, fig. 16) approach
that of H. linda, but their radulae are
quite different (Habe, 1952, pl. 21, figs.
28, 24).
In addition to the radula, the male
copulatory organ of Haminoea linda also
differs considerably from the corre-
sponding structures known in other
species of Haminoea. The Hancock’s
organ of H. linda is similar to that of
Lamprohaminoea cymbalum (Fig. 17).
5. Lamprohaminoea cymbalum (Quoy
and Gaimard, 1833)
(Figs. 17-20)
Pilsbry, 1895, p 367, pl. 40, figs. 6, 7;
Bergh, 1901, p 230-231, pl. 19, figs. 6-
8; Pruvot-Fol, 1934, p 25; Habe, 1952,
publ; pl 20, figs 153) Zilch; 1959, Up
43, fig. 141.
Occurrence: Reef on South end of
Parry Island. Part of our specimens
were collected by Prof. H. van der
Schalie.
Further distribution: Kerimba Is-
lands, northern Mozambique; Reunion;
Mauritius; Port Lincoln, South Aus-
tralia; Nagasaki, southern Japan; Guam,
Mariana Islands (original locality); New
Caledonia.
The height of our shells measured up
to 12 mm and the greatest breadth,
Slightly anterior to the middle part ofthe
shell, was 7.2 mm. The shell has 1 1/2
whorls, is subglobose, fragile, pellucid,
white and narrowed posteriorly. Growth
lines are distinct in some shells, but
may not be developed in others. The
aperture is wide in front, narrowed
behind. The outer lip is slightly con-
vex, overtops the apex, rising from the
center of the sunken spire. The columella
is deeply concave; its basal callus forms
a narrow reflection over the inner lip.
The length of preserved, well an-
esthetized adult animals is about 18
mm, their breadth 9 mm. Their color
in life is bright green with bright orange
spots. The mantle of preserved snails
when removed from their shells shows
large light spots and small brown and
orange ones. The cephalic shield is
244 MARCUS AND BURCH
notched in front, bilobed behind. The
parapodia are scarcely halfas long as the
shell. Hancock’s organ (Fig. 17) is a
simple undulated ridge, as in the pre-
ceding species.
The jaws of Lamprohaminoea cym-
balum consist of rodlets which measure
6 micra in diameter. The radula studied
(Fig. 18) comprises 36 rows and 14
lateral teeth per half-row. The
rhachidian tooth is high, with a smooth
base and a long median cusp flanked by
two smaller ones. The lateral teeth
are rather uniform; all lateral teeth,
including the first lateral, lack denticles
on their cusps. The cusp is longest in
the middle of the half-row. The gizzard
plates are chestnutbrown, with 17 smooth
ridges.
The atrium in Lamprohaminoea cym-
balum (Fig. 19, A) is long, muscular
and without a special sheath. The fibers
of the penial retractor muscle (RMu)
insert on the inner end of the atrium.
Entally to the atrium the male duct has
a spiny, strongly muscular section (Fig.
20, Pe) and farther inward a smooth,
thin-walled section (MD). For a part
of its course this thin section is em-
bedded in the retractor fibers (RMu); it
opens into the prostatic gland (Pr).
The prostate gland is sausage-shaped,
entirely glandular, undivided and without
a separate seminal vesicle.
Discussion of Lamprohaminoea
cymbalum
This species approaches Haminoea
linda in the similarity of its simple
Hancock’s organ and the absence of a
penial papilla. Both species have a
Spinous loop in the male duct. In dH.
elegans there are many rows of spines
on the penial papilla (Marcus, 1958b,
figs. 18-20).
6. Dolabrifera dolabrifera (Rang, 1828)
Marcus, 1963, p 10 (bibliography).
Occurrence: Under rock on seaward
tide flat at the north end of Parry Island,
March 25, 1960.
Further distribution: Circumtropical
and circumsubtropical, but not yet
recorded from the American Pacific
coast.
According to Engel’s revision (1936,
p 29-43) only Dolabrifera nicaraguana
Pilsbry, 1896 (p 124) from the west
coast of CentralAmericaand D. varie-
gata (Risbec, 1928b, p 54) from New
Caledonia are valid species of the genus
besides D. dolabrifera. Pruvot-Fol
(1954, p 13) considers the subequal
prongs of the lateral radular teeth of
her material from Tahiti, Society Is-
lands, a distinction separating it from
D, dolabrifera, but Eales (1944, p 7-8,
fig. 9A) shows similar characters to
occur also in D. dolabrifera. Farran’s
(1905) maillardi Deshayes, 1863, whose
name Pruvot-Fol uses, was united with
D. dolabrifera by Engel (p 39).
The shell and male copulatory organ
of the material from Eniwetok agree with
D. dolabrifera, and the lateral teeth of
the radula have subequal prongs.
7. Stylocheilus longicauda (Quoy
and Gaimard, 1824)
Engel, 1927, p 105-107, figs. 17-25;
1936, p 55-72, figs. 24-43; Marcus,
1963, p 11-15, figs. 10-21.
Occurrence: In tide flats of Eniwetok
Island, March 4, 1960.
Further distribution: Circumtropical;
not yet recorded from the west coast of
America.
Preserved specimens measure about
35 mm in length. Living animals exhibit
long tails andarborescent papillae. They
are brownish with fine dark longitudinal
striae, white spots, and a few blue
ocelli. This color pattern andthe spines
of the penis are characteristic of Stylo-
cheilus longicauda.
8. Chromodoris fidelis (Kelaart, 1859)
(Fig. 21)
PACIFIC EUTHYNEURA 245
Doris fidelis Kelaart, 1859, p 295.
Chromodoris flammulata Bergh, 1905,
DOI Ё52. ipl. 4, 15-9, pl. 16, figs:
16-19; Risbec, 1928a, p 137, fig. 35, pl.
8, fig. 8.
Chromodoris lactea Bergh, 1905, p
159-160, pl. 16, figs. 40-43.
Chromodoris fidelis Eliot, 1906a, p
642-643, pl. 42, fig. 2; 1909, p 91-92.
Glossodoris fidelis Risbec, 1953, p 66;
Baba, 1953, p 208, figs. 4, 6, H-I.
Occurrence: Under rock at about 3 m
depth on lagoon side near shore of
Eniwetok Island; collected by Mr.
Richard Willis, March 27, 1960.
Further distribution: Ceylon (original
locality); Malay Archipelago, East coast
of Sumbawa and Kwandang Bay, North
coast of Celebes; Seto, Kii Peninsula,
Japan; New Caledonia.
The living animal extends to 30 mm,
and at such a length has a width of 6
mm. The broad fore end is nearly
straight. The short triangular tail pro-
trudes from under the mantle. The
border of the mantle is slightly wavy;
its front and sides are somwhat broader
than the body.
‘The notum and underside of Chromo-
doris fidelis are pale creamy white. The
edge of the back is yellow with about 20
maroon projections of different lengths
entering the creamy notum. The maroon
projections are edged by a fine thread
of opaque white.
The tentacles are short and digitiform.
The rhinophores are about 4 mm high,
with 15-16 dark orange lamellae which
are lighter toward the tip of the rhino-
phore. The stalks of the rhinophores
are rather transparent, but opaque
whitish on the inside. There are 5 uni-
pinnate, whitish gills, the front one
shorter than the others.
The foot of Chromodoris fidelis has
acute lateral angles in front; it is
widened in the posterior third, lanceolate
behind.
The labial armature consists of short,
| bifid and bent rods which stand in rows.
The radula contains 45 rows with 42 teeth
| in the half-row. The rhachis is naked,
| without thickenings or false plates.
The eggs in the spawn show dark
yellow caps directed towards the
beginning of the egg string on larger
light yellow spheres.
Discussion of Chromodoris fidelis
The synonymy given above is that
presumed by Eliot (1909) and maintained
in Pruvot-Fol’s (1951, p 103, 104, 114)
revision. The unusual appearance ofthe
labial armature occurs in Eliot’s
material from the original locality and
in our material from Eniwetok. This
character has not been mentioned by
Bergh, Risbec or Baba. Eliot’s material
from Ceylon had traces of triangular
thickenings on the rhachis. In C. flam-
mulata the rhachis is naked as it is in
our material. In C. lactea and in Baba’s
Specimens there is a small, though dis-
tinct, rhachidian tooth. Risbec did not
describe the rhachis. Pruvot-Fol (1951,
p 77-78) considers the presence or
absence of radular elements on the
rhachis as systematically insignificant;
therefore, her synonymy was adopted
here, though with some doubt.
Doris preciosa Kelaart, 1858 (year
according to O’Donoghue, 1933, p 226)
is systematically near Chromodoris
fidelis. The rhinophores and gills of С.
preciosa are red or black (Eliot, 1909,
p 92) and evidently the color of these
organs varies also in C. fidelis. They
were described as black or dark violet,
but are dark orange in our material.
C. lata Risbec, 1928, which, as Pruvot-
Fol indicates, approaches C. fidelis in
characters, is maintained as a distinct
species by Risbec (1953, p 74).
9. Chromodoris briqua, new species
(Figs. 22-24)
Occurrence: Eniwetok Atoll; collected
by Mr. Richard Willis, March 27, 1960.
The animal is broadly elliptic, evenly
rounded in front and behind (Fig. 24).
Length of living, but not crawling, slug
is about 32 mm, its breadth 16mm. The
free mantle border is 4 mm broad on
either side, covering the head and hind
246 MARCUS AND BURCH
FIG. 21. Chromodoris fidelis. FIGS. 22-24. Chromodoris briqua, п. sp. FIGS. 25-27. Hypselodoris ©
hilaris. Fig. 21. C. fidelis, living snail drawn from Kodachrome transparency, side view. Fig. 22. Radular
teeth of C. briqua. Fig. 23. Labial rods. Fig. 24. Ventral view, from living animal. Fig. 25. Dorsal view
of crawling slug of H. hilaris, drawn from Kodachrome transparency. Fig. 26. Radular teeth. Fig. 27.
Labial armature.
end of the foot when the animal is at The notum is smooth, without spicules
rest. The outline of the mantle is in the animal put directly into 70% ethyl
slightly fringed, the undulation more alcohol. The general color of the living
pronounced in the preserved specimen. animal is yellowish-orange (actually a
PACIFIC EUTHYNEURA 247
yellow background with red spots). The
notal margin has a narrow outer, light
blue stripe accompanied by a broader
inner, deep purple one. The underside of
the mantle and the sole are yellow; in
addition to the blue and purple lines
noted above, the underside of the mantle
has a third, narrow, innermost maroon
one.
The tentacles are orange, digitiform;
the rhinophores maroon, speckled with
white, their 28-30 lamellae disposed
horizontally in the preserved specimen.
There are about 10 unipinnate gills, on
one side of which are some Secondary,
probably regenerated, plumes. The an-
terior border of the branchial pocket is
raised; the color of its membrane and
center is yellow. The gill leaves are
maroon ringed with white. The anal
papilla has 4 rings of white spots.
The foot is evenly rounded in front
and behind in the living quiescent slug;
in the preserved specimen a blunt tail
protrudes from under the mantle. The
anterior pedal border is transversely
grooved, without a notch. The lateral
pedal corners are rounded, not expanded.
‘The labial cuticle of Chromodoris
briqua has a _ dorsally interrupted
grasping ring constituted of dark red
curved rods (Fig. 23) with a simple,
exceptionally bifid, tip. The radula
(Fig. 22) has 54 rows, each row witha
rhachidian tooth and 63-64 teeth per half-
row. The central tooth is rather strong,
50 micra high, with abroadly triangular,
wavy edged cusp measuring 13 micra.
The innermost lateral tooth is about 80
micra high, its short cusp having 2 broad
inner and 5 small outer denticles. The
second lateral tooth is a little higher
and with a longer cusp and without inner
denticles. The cusp grows successively
longer onthe outer lateralteethandbears
up to 8 outer denticles. The height of
the base attains 104 micra in the 12th
lateral tooth. High, hook-shaped lateral
teeth continue outwards; the outermost
10 teeth decrease in height and length of
cusp, becoming laminar with a den-
ticulate edge.
The gonad appears as a cap on the
front of the intestinal gland; itsampulla
is distended by sperm. The male duct
has a proximal, much convoluted, soft
prostatic part and a straighter distal
one. It appears silky, due toits muscular
sheath. The spherical spermatheca and
the pyriform spermatocyst are attached
to one another at the proximal end ofthe
vagina. Near this point the fertilizing
(uterine) duct leaves the vagina. The
male and vaginal apertures are united
on the genital papilla, with the nidamental
opening immediately behind it. A vesti-
bular gland, an organ not constantly
occuring in Chromodoris (see Odhner,
1934, p 250-251) was not found.
Between the epidermis and the body-
wall musculature are soft white and red
spherules, probably glands, and a white,
fibrous network.
The name of the species is derived
from “brique” = brick.
Discussion of Chromodoris briqua
The specimen was compared with all
species of Pruvot-Fol’s revision (1951)
and with the Indo-Pacific ones later
described by Baba (1953), Burn (1957;
1961; 1962), Farmer (1963), Gohar and
Aboul-Ela (1957), Pruvot-Fol (1954) and
Risbec (1956).
The Chromodoridinae have either a
naked rhachis, a thickening of the cuticle,
or a dwarf central tooth with or without
a cusp. Chromodoris briqua has a
dwarf central tooth with a cusp. Species
in which the rhachidian tooth is of normal
or nearly normal height, and has a pro-
jecting cusp (genera Cadlinella, Lisso-
doris and Risbecia; see Odhner, 1934,
p 247-249), and those species in which
the cups of the rhachidian tooth is split
into subequal denticles, are nowexcluded
from the genus Chromodoris (Pruvot-
Fol, 1951, p 77). However, a subfamiliar
separation between a projecting cusp (in
Cadlinellinae) and a subdivided one (in
Chromodoridinae) is not recommendable
(Marcus, 1959, p 33). The difference
between an entire cusp (C. amoena
Cheeseman, see Odhner, 1934, text fig.
248 MARCUS AND BURCH
14) and a denticulate one (С. juvenca
Bergh, 1898, pl. 31, fig. 7) is reducedby
the wavy edge of the rhachidian cusp in
C. briqua.
The presence or absence of a tooth-
like structure on the rhachis is in many
cases a specific character. A contrary
conclusion may be inferredfrom White’s
discussion (1951, p 244) of C. runcinata
Bergh, but actually she slipped into
O’Donoghue’s description (1929, p 820)
of С. inornata Pease. There are only
a few species of Chromodoris with a
dwarf, cusp-bearing rhachidian tooth and
we will mention several examples: C.
alderi Collingwood, 1881; C. amoena
Cheeseman, 1886; andC.aureopurpurea
Collingwood, 1881, and refer to Baba
(1949, text figs. 52, 54) and Odhner (1934,
fig. 14) for their radulae. Bergh (1892,
p 1110) united C. alderi with C. reticu-
lata (Pease, 1866). He was followed by
Eliot (1904, p 386), Farran (1905, p 341),
Baba (1933, p 169), and Allan (1947, p
444), though not by Pruvot-Fol (1951,
Species nos. 11 and 168).
The combination of the radula with the
labial armature and the broad mantle
having a bicolored border warrant a
Specific distinction for Chromodoris
briqua. According to Haefelfinger (1959)
the color marks seem to be even more
specific than is frequently assumed. The
above-mentioned subcutaneous spher-
ules also occur in other Chromodoridinae
(Pruvot-Fol, 1954, p 25-26).
10. Hypselodoris hilaris (Bergh, 1890)
(Figs. 25-27)
Chromodoris hilaris Bergh, 1890, р
935-9375 ple 865 fies. 11-155) ©: hr var.
Eliot, 1904, p 396.
Chromodoris lineata Eliot,
396-397, pl. 24, fig. 7.
Glossodoris hilaris Baba, 1953, р 210-
211, figs. 5, 6, J-K; Risbec, 1956, p 9.
1904, p
Occurrence: Eniwetok Atoll, Annai-
anni Island, in water about 2 m deep,
on the edge of a large stone in lagoon
about 7 m from shore.
Further distribution: Zanzibar; Bay
of Suot, Nhatrang, Vietnam; Ambon
(original locality); Seto, Kii Peninsula,
Japan.
The animal (Fig. 25) measures 40mm
in length and 5 mm in width when
stretched out and crawling. Itis rounded
and sometimes broadly expanded in front,
pointed behind. The free border of the
mantle is a little broader than the foot;
it covers the head of the crawling slug,
leaving the tapering tail free.
The color is white with 5 reddish-
purple longitudinal lines on the notum
and one around the margin. These
lines are united by irregular transverse
connections. In the living and the pre-
served specimen the white areas between
the dark meshes are a little raised. The
color markings of the head, tail, and
the post-branchial area are shown in
Fig. 25. The notum contains small
papillae which are probably outlets of
glands. As in many Chromodoridinae
(see Marcus, 1955, p 126), there are
3 rows of light glands on the hyponotum.
There is a lavender band on the edge
of the foot which shows through in ventral
view.
The tentacles of Hypselodoris hilaris
are digitiform and white with lavender
bases. The same lavender pigment
occurs along the anterior border of the
foot. The rhinophores are 4 mm high,
with 15 lamellae, and deep orange in
color, except at the tips, where they
are white. In front of the rhinophores,
where the eyespots show through, the
pigment is lighter. There are 10 uni-
pinnate gills; their afferent (inner) sides
are white, their efferent (outer) sides are
orange.
The foot has a transversely grooved
anterior border, without a notch. The
lateral angles of the foot are marked,
though not projecting.
The labial cuticle (Fig. 27) is
strengthened in 2 lateral areas which
are connected by a thinner median zone,
that bears simple scale-like platelets.
The same type of platelets occur also
PACIFIC EUTHYNEURA
on the low marginal parts of the thickened
areas. The tips of the central rods are
subdivided into a long cuspand2 smaller
ones, one of which is stronger than the
other. The radula (Fig. 26) comprises
about 72 rows, with about 55 teeth per
half-row. The rhachis is naked. Most of
the teeth are bicuspidate, with the upper
cusp longer than the lower one. The
innermost tooth of each half-row has up
to 4 inner and 6 outer denticles. The
other teeth have only outer denticles.
About 5 of the marginalteethare laminar
and have a single cusp followed by some
denticles.
Discussion of Hypselodoris hilaris
The present material differs from
Chromodoris briqua inhaving more color
marks on the tail and stronger con-
nections between the longitudinal lines
of the notum. The type has only 4
longitudinal lines on the notum, 2 on
either side of the middle.
Eliot’s above-mentioned Chromodoris
lineata (1904) is H. hilaris (Baba, 1953).
Later, Eliot (1910, p 430) pointed out
the resemblance of Doris magnifica Quoy
and Gaimard, 1832, and D. lineata Eydoux
and Souleyet, 1841, to H. hilaris. The
former is identical with Chromodoris
quadricolor (Rüppell and F. S. Leuckart,
1828) (see Pruvot-Fol, 1934, p 71-72).
The 5 violet lines on the back of С.
lineata are raised (see Barnard, 1927,
p 183). The labial armature and the
radulae of the original specimens were
not described. Therefore, the name
lineata cannot replace hilaris.
Pruvot-Fol (1951, p 84) thinks that
Chromodoris alderi Collingwood, 1881,
might be the full-grown stage of H.
hilaris, but C. alderi has unicuspidate
radular teeth, hence is a Chromodoris
as defined by Odhner (1957), not a
Hypselodoris.
11. Gymnodoris bicolor (Alder
and Hancock, 1864)
Trevelyana bicolor Alder and Hancock,
1864, p 440, pl. 29, figs. 11, 12.
249
Gymnodoris bicolor Macnae, 1958, p
358-359 (full synonymy; add:
Trevelyana bicolor ? Eliot, 1904, p 89,
pl. 4, figs. 1a-c).
Occurrences: (1) Under stone on the
seaward tide flat at the central part of
Parry Island; March 23, 1960; (2) on
north end of Japtan Island, March 28,
1960.
Further distribution: Inhaca, Delagoa
Bay, Mozambique; Zanzibar; Ceylon;
near Madras (original locality); Viet-
nam; Japan, from Sagami Bay to southern
Kyushu; Palau Islands; New Caledonia;
Samoa (Eliot, 1899, p 520).
One of the larger specimens was 15
mm long and 4 mm broad when crawling,
stretching out attimesto19x3mm. The
back is orange or yellow with tiny bump-
like or spike-like papillae which have
orange tips. Subepidermal yellow glands
also occur on the back. The frontal
veil is broadly rounded, its edge has a
dozen short languettes of different sizes.
The tail is pointed.
The tentacles are short but extensible
and are inserted on the oral disc which
is connected with the anterior border of
the foot. The rhinophores have about
15 lamellae and are yellow with orange
tips. There are black eyespots between
the posterior borders ofthe rhinophorial
pockets. One specimen had coalesced
rhinophores (see also Hoffmann, 1933,
p 216-217). The genital papilla is at the
level of the anterior border of the
branchial pocket. There are 10gills, the
anterior ones slightly larger than those
flanking the anus.
Our specimens of Gymnodoris bicolor
had no labial plates. The radula of the
examined specimen had 20 rows of teeth
with about 25 teeth per half-row. The
rhachis was naked. The innermost
lateral tooth is brown, bigger than the
following colorless teeth. The cusp ofthe
second tooth is a short sharp point rising
from a wide base as figured by Bergh
(1877, pl. 56, figs. 19-23) and Baba
(1949, text fig. 35). The bases of the
following teeth are narrower than the
250 MARCUS AND BURCH
base of the second, but they are also
strong. Their cusps are long, nearly
straight and slightly curved at the tip.
A few outermost teeth are smaller.
The smaller slug (from Parry Island)
was observed biting the larger one
(from Japtan Island) in the genital region.
The latter specimen was preserved with
everted penis. Risbec (1928a, p 188-
189, text fig. 57 bis) interpreted an
identical observation of the same Species
as an attempt of the animal inthe female
phase to squeeze sperm out of the gonad
of the slug in the male phase. Risbec
found non-synchronous development of
oögenesis and spermatogenesis as well
as simultaneous hermaphroditism in
Gymnodoris bicolor.
Discussion of Gymnodoris bicolor
The only originally described species
of Gymnodoris Stimpson (1855, p 379)
had 9 gills. It is certainly a Trevelyana
Kelaart, 1858, as understood by Alder and
Hancock (1864) and Bergh (1877; 1905).
The types of the closely related genera,
Nembrotha Bergh, 1877, p 450; Paliolla
Burn, 1958, p 7; and Tambja Burn, 1962,
p 98, have fewer gills. Vayssiére (1912,
p 8) suggested a subgeneric separation
of Trevelyana striata Eliot, (1908, p 100)
and Risbec (1928a, p 193) separated this
species from Gymnodoris by its color
marks as Analogium, a genus with 10
gills. Macnae (1958, p 355) doubted
whether Risbec’s genus was necessary.
Stimpson’s Species, Gymnodoris
maculata, from the Ryukyu Islands can-
not be defined without knowledge of its
radula. Therefore, the substitution of
Gymnodoris for Trevelyana (O’Donog-
hue, 1929, р 733) is debatable. But
since the most recent publications
(Risbec, 1956; Маспае, 1958; Baba,
1960a; Burn, 1962) all use Gymnodoris,
their example is followed here.
12. Dendrodoris nigra (Stimpson,
1855)
Doris nigra Stimpson, 1855, p 380.
Doridopsis nigra Alder and Hancock,
1864, p 128, pl. 31, figs. 13-16.
Doridopsis arborescens Collingwood,
1881, p 134-135, pl. 10, figs. 15-17.
Doriopsis nigra + nigra var. + nigra
var. luteopunctata Bergh, 1905, p 169-
172, pl. 24 ties. 13-14.
Dendrodoris nigra Baba, 1935, p 348-
349, text fig. 12, pl. 6, fig. 2; 1949, p
69, 154-155, pl. 26, figs. 98-99.
Occurrences: (1) Central part of Parry
Island; and (2) under stones at the north
end of Japtan Island. A total of 13
specimens were collected from March 23
until April 8, 1960.
Further distribution: Indo-West
Pacific Ocean from the Red Sea, Zanzi-
bar, and Mozambique to the Abrolhos
Islands, West Australia; Sydney (D.
melaena Allan, 1932, p 98; name
corrected by hand in the copy received
in 1954 from Mrs. Allan), and Japan
(from the Ryukyu Islands to Mutsu Bay,
Lat. 40° 52’ N). Also from the Gilbert
Islands (material of the U. S. Nat. Mus.,
seen by E. Marcus) and New Caledonia.
Length of the animal is 8-35 mm.
The color of the notum is black with
white spots occurring singly or in
clusters. There is an inner red and an
outer black border in some specimens.
The tips of the rhinophores are white,
the border of the foot reddish. The
anal papilla is in the mid-line, a little
behind the circle of gills.
A spiral egg-ribbon, faint yellow, 2
mm high, 10 mm in diameter, was
spawned by a 25 mm-long slug.
13. Dendrodoris erubescens (Bergh,
1905)
Doriopsis erubescens Bergh, 1905, p
173-174, pl. 3, fig. 15.
Dendrodoris communis Risbec, 1928a,
p 67-69, text fig. 7, pl. A2 (p 114), pl. 1,
fig. 6.
Dendrodoris erubescens Risbec, 1953,
p 22-23, figs. 2 d-i, fig. 4; 1956, p 26-
Ре
Occurrence: Japtan Island, under
|
PACIFIC EUTHYNEURA
rock, seaward tide flat, 1 specimen,
collected by Dr. William H. Heard on
March 8, 1960.
Further distribution: Vietnam; Sala-
jar Island, Flores Sea (originallocality);
New Caledonia.
This is a small species, our speci-
men measuring 8.5 mm in length. The
notum is pale pink, the central area
darker, more orange. There are about
10 raised spots on the notum, which
were colored orange with white centers.
The anal papilla completes the circle
of gills, which comprises 2 branchial
buds and 6 brownish gills. The gillsare
unipinnate, although one of them is
beginning to develope secondary
pinnules.
D. erubescens is similar to D. rubra
(Kelaart, 1858) which ranges from the
Red Sea to Japan and is mentioned in
most reports from the Indian Ocean,
e.g. by Alder and Hancock (1864, p 126,
pl. 31, figs. 1-2); frequently D. rubra
is described and figured as somewhat
spotted. Since Bergh (1905, p 176),
as well as Risbec (1956, p 22), both of
whom failed to refer to this similarity
in color, classified D. rubra as well as
D. erubescens, these two species are
probably distinct.
14. Herviella claror Burn, 1963
(Figs. 28-30)
Burn, 1963, p 18-19, figs. 11-15.
Occurrence: North end of Eniwetok
Island on the lagoon side, under sub-
merged rocks in about 10 cm of water
at low tide. The 3 specimens were
collected by Dr. William H. Heard,
April 2-12, 1960.
Further distribution: Woody Head,
north of Clarence River Heads, north-
ern New South Wales.
The length of the adult living animal
is about 8 mm. The body is slender,
ending in a long pointed tail (Fig. 28).
The general color is light yellow; the
back is speckled with single large
251
melanophores. There are white trans-
verse bands between the rows of cerata.
The rhinophores and the basal 2/3 of
the tentacles are speckled with black;
the tips of the tentacles have opaque
white granules. The cerata are white
with an orange ring in the upper third.
The yellowish-gray diverticula of the
intestinal gland shine through the cerata.
The tentacles and rhinophores of Her-
viella claror are smooth, of about equal
length. The foot is rounded in front,
bilabiate, broader than the head. The
cerata are fusiform, forming 4 rows, the
foremost of which belong to the right
and the left anterior “liver.” The rows
contain 3, 4,2 and2cerata, respectively,
from front to rear. The genital aperture
is under the first row of cerata, the
anus close behind the second row.
The jaw (Fig. 30) is oval in shape and
horn-colored. The masticatory process
is short with 6 big, inclined denticles.
There are 11 horseshoe-shaped radular
teeth; each has a broad median cusp
and 3-4 strong denticles on either side
(Fig. 29).
Discussion of Herviella claror
The type species of Herviella Baba,
1949 (p 107, 180), is H. yatsui (Baba,
1930 1937. р 328. pl. 2, fie. .2) from
the Pacific coasts of middle and southern
Japan. Other species are Н. affinis
Baba (1960b, p 81) from the Sea of
Japan (Toyama Bay) and the Pacific
coast (Osaka Bay) of Japan, H. exigua
(Risbec, 1928a, p 245; 1953, p 134)
from New Caledonia, and H.claror Burn,
1963, from the east coast of Australia
(290 20’ S). H. exigua differs from the
other species by lateral denticles of equal
length on the radular tooth. dH. yatsui
and H. affinis have more slender cerata
than the Australian H.claror and the
Eniwetok specimens; the proportion of
length to breadth of their jaws is 5:4
against 7:4 in H. claror including our
Specimens from Eniwetok. The number
of denticles on the masticatory process
is 7-12 in H. yatsui and 12 in A. affinis
in contrast to 6 in H. claror, including
252 MARCUS AND BURCH
y
29
yc
/
35
FIGS. 28-30. Herviella claror. FIGS. 31-35. Herviella mietta, n. sp. Fig. 28. Living slug of H. claror,
drawn from Kodachrome transparency, dorsal view. Fig. 29. Radular tooth. Fig. 30. Jaw and masticatory
denticles.
and from living animal.
Radular tooth.
our specimens. Therefore, the identi-
fication of the species from Eniwetok
with the geographically most distant one
is unavoidable.
15. Herviella mietta, new species
(Figs. 31-35)
Occurrence: North end of Eniwetok
Island on the lagoon side, in about 10
cm of water at low tide, under sub-
merged rocks (13 specimens), and Annai-
anni Island (3 specimens collected by
Dr. William H. Heard; April 2-12,
1960).
Fig. 31. Dorsal view of living slug of H. mietta, n. sp., drawn from Kodachrome transparency
Fig. 32. Right rows of cerata. Fig. 33. Penial stylet. Fig. 34. Jaw. Fig. 35.
Living animals measure 7-11 mm.
Their bodies are slender with pointed
tails (Fig. 31). Two color types are
represented in our material. The first
type is light and transparent, the back
is covered with white granules, the head
has a black pattern, there is a black
band on the rhinophores, some black
pigment on the tentacles, and the yellow
diverticula of the intestinal gland may be
seen in the cerata (which also have
white cnidosacs and, in their basal
third, brown pigment). The second color
type is dark, the back and the upper
part of the sides of the foot are black,
the rest of the foot and sole are white,
PACIFIC EUTHYNEURA
the tentacles have a narrow black longi-
tudinal stripe, there is a black band on
the rhinophores, there are light halos
around the eyes and between the
tentacles, and the cerata are black, with
a white cnidosac andthe yellowintestinal
gland showing through.
The smooth tentacles of Herviella
mietta are 1/3 of the body length. The
rhinophores are also smooth and a little
shorter. The foot is rounded in front
and bilabiate. The cerata are long and
fusiform, thinner than those of H. claror,
caducous, and arranged in 5-6 rows on
each side (Fig. 32). The first ceras of
each row is the smallest. The hind-
most cerata of one row cover the fore-
most cerata of the following row. All
rows of cerata are slightly curved, al-
though not arched in a horseshoe shape.
The first row (with 5-6 cerata) oneither
side represents the anterior liver. The
posterior liver branches have 6-3 cerata.
The genital opening is under the first
row and the anus is at the end of the
second row. In 1 specimen the brown
penial stylet (Fig. 33) projected from
the genital aperture. This stylet
measured 84 micra in length.
The jaw is dark, long and expanded
dorsally (Fig. 34). The masticatory
process bears 18 smooth denticles, the
hindmost of which is the largest. The
radular teeth (Fig. 35) are horseshoe-
shaped, 18 in number, with very strong
central cusps flanked on either side by
8-9 thin, pointed denticles. The denticles
first decrease and then increase in
length. The tips of the longest, outer-
most denticles curve slightly inward.
The name of this species is derived
from “miette” = trifle, crumb.
Discussion of Herviella mietta
The jaw resembles that of Caloria
(Facelinidae) or of Dondice (Favorinidae,
Facalaninae) andthe radular teeth, whose
long lateral denticles are somewhat
Similar to those of the pectinate tooth
of Cerberilla, are quite peculiar charac-
ters of the new species. It belongs to
those Favorinidae which have single
253
rows of cerata on the liver branches,
i.e., to the Favorininae (Marcus, 1958a,
p 59). Among the genera of this sub-
family (Marcus, 1960a, p 922, 924) only
Cratena Bergh, 1864 (according to
Lemche, 1964, Rizzolia), or Herviella
Baba, 1949, can perhaps receive the
present species. Its simple anterior
liver branches and the armed penis show
that it is better included in Herviella
than in Cratena, as defined by Macnae
(1954, p 29).
From the lateral view of the radular
tooth of Herviella yatsui (Baba, 1949,
text fig. 146B) it seems that in that
species also the outermost denticle is
longer than the inner ones. Moreover,
the general color of H. yatsui is also
extremely variable (Baba, 1937, pl. 2,
fig. 2; 1949, pl. 47, figs. 159-161).
16. Onchidella evelinae, new species
(Figs. 36-39)
Occurrence: In cracks in coral slabs
above water line (at low tide) on the
lagoon side at the north end of Eniwetok
Island, April 5, 1960.
The average length of the adult living
slugs (Fig. 36) is 6 mm, their breadth
4mm. Ina preserved animal4mm long
the sole is 2.5 mm broad; the hyponotum
of one side measures 1 mm. The mantle
is strewn with little raised warts, which
coalesce in part and contain glands.
Small nodules can be seen between the
warts. The general color of the notum
is yellowish, with the underlying dark
greenish intestinal gland showing through
the central part. The border of the notum
is lightly colored. There is dark pig-
ment particularly around the bases of
the warts, but their tops have very little
or no pigment. There are 16-20 pigment-
free marginal papillae. The hyponotum
and sole are whitish, the latter with
dark pigment in one specimen. The
hyponotal line is 0.6 mm from the edge.
Between the edge and the hyponotal line
are small glandular papillae. The skin
between the hyponotal line and the sole
254 MARCUS AND BURCH
is smooth.
The opening of the mantle cavity is
covered by the tip of the foot. The
female aperture is located to the right
of the mantle cavity opening. The dis-
tance of the pneumostome from the
border is about 1/4 of the breadth of
the hyponotum.
The peritoneum is not pigmented. The
jaw of a preserved 4 mm specimen is
0.2 mm broad, yellowish, and shaped
like that of other species, e.g., Onchidella
patelloides figured by Wissel (1904, fig.
77). The radula comprises 50-60 rows
with 40-48 teeth per half-row (Fig. 38).
The rhachidian tooth is tricuspid, its
median cusp the largest. Theinnermost
pleural tooth measured 16 micra high;
the one following it is 26. micra high.
The other pleural teeth are all nearly
the same size, decreasing gradually
toward the outside of the radula. The
terminations of the mesocones are
pointed; the points are worn in the
oldest 1/3 of the radula. The intestine
is like that of Plate’s (1893, p 121) 4th
type, but the descending limb is still
farther to the right than thatin O, celtica
(pl. 8, fig. 32). A sectioned slug, about
3 mm in length after preservation, has
a smooth lung. The right and left
halves of the kidney are symmetrical,
without lamellae. The recurrent limb of
the kidney runs ventrally to the right
half.
The above sectioned animal was inthe
male phase (Fig. 37). Sperms were
present in the ovotestis (o) and ampulla
(x) of the hermaphrodite duct (h). There
is no caecum (see Fretter, 1943, p 699)
in this species. The albumen glands (k)
and the mucus gland (m) are still small.
The vesicle of the bursa (b)is spherical,
its duct (s) long and winding. The lining
of the vagina (w) is folded. The ectal
section of the vagina is not widened in
comparison with the oviduct (u). The
prostate (q) is large, nearly cylindrical
and its lumen smooth, not folded.
The efferent duct approaches the skin
to the right of the female aperture. It
then courses forward along the right side
of the body. Under the right tentacle
the duct curves backward into the body
cavity, descending straight (d) along the
penis (Fig. 39). The wall of the duct
is muscular; its rather thick layer of
connective tissue contains vesicular
cells. The penis of a 4 mm slug
measured 2 mm in length and 0.1 mm
in diameter. The penial retractor
muscle (r) is about 0.6 mm and inserts
at the fundus of the penial pouch. It
originates a little behind the peri-
cardium (in Fig. 39 the retractor is
bent forward to save space). The penial
pouch contains the efferent duct (z),
which ends on the long (0.17 mm in
length) muscular papilla (p), and a long
diverticulum. The epithelium of the
diverticulum produces a solid cuticular
structure (t). This stylet, about 1.2
mm in length and 80 micra in diameter
near its inner end, is cylindrical,
lamellate below, and becomes semilunar
in transverse section farther in front.
Its axial thickenings and flat shape at
the level of the penial papilla are shown
in transverse sections in Fig. 39. Con-
spicuous vesicular cells can be seen in
the conjunctive tissue in the ectal third
of the penial pouch (y).
The species is namedfor Mrs. Eveline
du Bois-Reymond Marcus.
Discussion of Onchidella evelinae
Following a recent record (Solem,
1959, p 37), Taylor and Sohl (1962, p
13) indicate one family of the Onchidiacea
with 6 genera and subgenera, but actually
there are 2 families with a total of 15
genera and subgenera (Marcus, 1960a,
p 876). The present species is defined
as belonging to the Onchidellidae and to
Onchidella Gray, 1850, by the position
of the male opening to the right of the
right tentacle, and the hyponotal line,
respectively. Hoffmann (1929, p269) sub-
divided Onchidella into Onchidella and
Occidentella according to the position of
the recurrent renal limb, ventral to the
kidney in the first and dorsal to it in
the second subgenus. Two notogaeic
Species, O.obscura (Plate, 1893), a
PACIFIC EUTHYNEURA 255
FIGS. 36-39. Onchidella evelinae, п. sp. FIGS. 40-43. Siphonaria guamensis. Fig. 36. Dorsal view of
living slug of O. evelinae, drawn from Kodachrome transparency. Fig. 37. Diagram of reproductive organs,
ventral view. Fig. 38. Radular teeth. Fig. 39. Male copulatory organ and sections of stylet; b, bursa; d,
efferent duct; h, hermaphrodite duct; k, albumen gland; m, female gland mass; o, ovotestis; p, penial
papilla; q, prostate; r, retractor; s, spermathecal duct; t, cuticular stylet; u, oviduct; w, vagina; x,
ampulla; y, penial pouch; z, efferent duct within penis. Fig. 40. Jaw of S. guamensis. Fig. 41. Reproductive
organs. Fig. 42. Elements of jaw. Fig. 43. Radular teeth; a, atrial thickening; f, flagellum; g, gland of
epiphallus; h, hermaphrodite duct; m, female gland mass; о, ovotestis; $, spermathecal duct; у,
seminal vesicle.
256 MARCUS AND BURCH
synonym ofnigricans (Quoy and Gaimard,
1833), and O. reticulata (Semper, 1882)
have a dorsal recurrent limb (Plate,
1893, p 132, 205, 208), and therefore
Hoffmann (l.c.) called Occidentella an
Australian group. The dorsal limb dis-
tinguishes them from О. evelinae, a
typical Onchidella. Of 2 other West
Pacific species, O. patelloides (Quoy
and Gaimard, 1833) and O. flavescens
(Wissel, 1904), the anatomy of the kidney
is not known. The first differs from O.
evelinae by its black peritoneum (Hoff-
mann, 1928, p 90), and the second by its
narrow sole (Wissel, 1904, p 668), whose
breadth is equal to that of the hyponotum
of one side. In his recordofO. maculata
(Plate, 1893) from New Guinea, Labbé
(1934, p 78) did not give details of the
kidney. If his specimen really was O.
maculata, previously known from the
coast of Southwest Africa, it would have
a ventral recurrent renal limb, like O.
evelinae. But in Labbé's and Plate's
maculata the unarmed penis contains
calcareous concretions, absent in O.
evelinae which has a cuticular stylet.
The male copulatory organ furnishes
the principal elements for the specific
classification of Onchidella, hence
specimens in the mature male phase
should be examined. On the other hand,
it is advisable to section small slugs
with incompletely developed female
glands. In big animals these are the
bulkiest organs of the genital system,
and often render the reconstruction
difficult. The absence of folds in the
lung (Marcus, 1956, p 79) of small
Specimens cannot be used for differ-
entiating species.
17. Stphonaria (Sacculosiphonaria)
guamensis Quoy and Gaimard, 1833
(Figs. 40-43)
Hubendick, 1945, p 25-27, fig. 33; 1946,
p 41, pl. 6, figs. 30-32.
Occurrence: Southend of Parry Island,
on rocks in the intertidal zone of the
lagoon.
Further distribution: Billiton, Java
Sea; Guam, Mariana Islands (original
locality).
The shells of this species measure up
to 12 mm in length, 9.1 mm in width,
and 5 mm in height. The shells are
rather symmetrical. The apex isbehind
the middle, very slightly recurved, and
worn in our specimens. There are 20-
26 principal ribs, low, slightly un-
dulating, with a secondary rib sometimes
between the two principal ones.
Our specimens exhibit considerable
variation in size. In all shells the ribs
are white, their interspaces dark gray.
The apex is light in many of these speci-
mens, and the remaining parts of the
surface are darker. Four of the shells,
however, have a dark apex and quite light
borders; 3 are more or less uniformly
dark, except for the ribs. The body
appears grayish when preserved in
formalin, not yellow as in Hubendick’s
(1945) material. The siphon cannot be
seen from the back.
The jaw (Figs. 40, 42)is semicircular;
its scaly elements are renewed from
time to time. The radula (Fig. 43)
comprises about 110 rows, the older
of which are procoelous, the younger
ones straight. The basal plate of the
rhachidian tooth is relatively broad and
terminates concavely or is nearly split.
Its short cusp is simple. There are up
to 36 teeth per half-row. The inner-
most has the usual strong socket anda
long cusp and is bifid at its tip. The
length of these points varies; frequently
the inner one is a little longer. The
basal plate is asymmetrical, prolonged
outward. The other lateral teeth are
Similar and decrease gradually in size
toward the outside of the radula. An
ectocone appears on the 13-15th tooth,
and an entocone appears on the 19th.
The 2 mesocones coalesce, forming a
rectangular plate in the outer half of the
half-row. The outermost or marginal
teeth are low and simplified.
The kidney is similar to Hubendick’s
PACIFIC EUTHYNEURA 257
(1945, p 35, fig. 61) B-type. The repro-
ductive organs (Fig. 41) are like those
shown by Hubendick (1945, fig. 33). Minor
differences are athickening ofthe genital
atrium (a) near the entrance of the
spermathecal duct (s), a slightly longer,
curved flagellum (f), and a more bulky
epiphallus gland (g). The black seminal
vesicle (v), not yet recorded for S.
guamensis, lies at the entrance of the
hermaphroditic duct (h) into the female
gland mass (m), as in the other species
of Siphonaria (Hubendick, 1945, p 11).
The receptacle and the filiform part of
the spermatophore are easily dis-
tinguishable from one another; thelatter
has no barbs.
Discussion of Siphonaria guamensis
The shape of the radular teeth and
their number are of restricted value in
the systematics of Siphonaria. The
kidney of the present species is ex-
ceptional in the subgenus Sacculosiphon-
avia, the other known species of which
have the C-type (Hubendick, 1945, p 35;
1946, p 41-42). The reproductive organs
are, together with the general charac-
ters of the shell, decisive for the
classification in this subgenus. The jaw
of S. guamensis differs widely from that
of S. cochleariformis (Hubendick, 1945,
fig. 86) of the same subgenus.
LITERATURE CITED
MADAM, W. and LELOUP, E., 1938,
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EUTHYNEURE MEERESGASTROPODEN VOM ENIWETOK ATOLL, WESTPAZIFIK
Die Arbeit beruht auf einer Sammlung euthyneurer Meeresschnecken des zweiten
Verfassers vom Eniwetok Atoll, Marshall Inseln. Vom Februar bis April 1960 wurden
17 Arten gesammelt, von denen 5 als neue Arten in dieser Arbeit beschrieben werden.
Die neuen Arten sind: Haminoea musetta, H. linda, Chromodoris briqua, Herviella
mietta und Onchidella evelinae. Von den übrigen 12 Arten erstreckt sich die Ver-
breitung von 7 vom westlichen Indischen Ozean (2 kommen auch im Roten Meer vor)
ostwärts bis Eniwetok oder noch weiter nach Osten; 2 Arten sind zirkumtropisch
oder zirkumsubtropisch, 2 Arten kennt man nur aus dem Westpazifik, und 1 Art ist
von Eniwetok westwärts bis in den östlichen Indischen Ozean verbreitet. Eine gewisse
Einförmigkeit der indowestpazifischen Riff-Fauna zeigt sich darin, dass 9 (oder mehr
als 50%) unserer Arten von der westlichen Grenze des Indischen Ozeans bis zum
westlichen oder zentralen Pazifik vorkommen. Die Gattung Herviella scheint auf den
Westpazifik beschränkt zu sein. Das notogäische Vorkommen einer Onchidella mit
ventral vom Hauptteil gelegenem rückläufigem Nierenschenkel ist bemerkenswert,
wie auch das kutikulare Stilett in einem Blindsack der Penis-Scheide.
RESUMEN
GASTROPODOS EUTINEUROS MARINOS DEL ATOLL ENIWETOK,
PACIFICO OCCIDENTAL
Este estudio se basa en una colecciön de Eutineuros marinos hecha por el segundo
autor en el Atoll Eniwetok, Islas Marshall, durante febrero-abril de 1960. Se
colectaron 17 especies, de las cuales las cinco siguientes se describen como nuevas:
Haminoea musetta, H. linda, Chromodoris briqua, Herviella mietta, y Onchidella
evelinae. De las otras 12 especies, 7 extienden su distribuciön hacia el este desde
el Océano Indico occidental (2 también aparecen en el Mar Rojo) a Eniwetok o mas
hacia el este; 2 especies son circumtropicales o circumsubtropicales; 2 se conocen
del Pacifico occidental solamente; y 1 se distribuye desde Eniwetok hacia el oeste,
dentro del Océano Indico oriental. La relativa uniformidad de la fauna de los arre-
cifes del Indopacifico occidental, está indicada por el hecho de que 9 (más del 50%)
de nuestras especies se conocen distribuidas desde el margen oriental del Océano
du Golfe d’Aden, 2me partie (suite et text-figs. | Berlin-Nikolassee, Gebr.
fin). Ann. Fac. Sci. Marseille, 20 Borntraeger.
(1911, Suppl.): 5-158, pls. 1-11.
ZUSAMMENFASSUNG
262
MARCUS AND BURCH
Indico al Pacifico occidental o central. La presencia notogeica de una Onchidella
con un limbo ventral recurrente del riñón y un estilete cuticular en el divertículo
de la cámara penial es müy notable.
RESUMO
EUTINEUROS GASTRÓPODOS MARINHOS DO ATOLL ENIWETOK, PACÍFICO
OCIDENTAL
O presente estudo baseia-se numa colecdo de moluscos marinhos eutineuros feita
pelo segundo autor no atoll de Eniwetok, nas Ilhas de Marshall, em fevereiro-abril
de 1960. Foram coletadas 17 espécies das quais 5 зао descritas como novas no
presente trabalho. As novas espécies sao: Haminoea musetta, H. linda, Chromodoris
briqua, Herviella mietta, Onchidella evelinae. Das 12 espécies restantes, a distri-
buigao de 7 estende-se do Indico ocidental (2 ocorrem também no Mar Vermelho)
até Eniwetok ou mais para o leste; 2 espécies зао circumtropicais ou circumsub-
tropicais; 2 espécies conhecem-se sömente do Pacífico ocidental, e 1 espécie осогге
de Eniwetok para o oeste, até ao Indico oriental. Certa uniformidade da fauna dos
recifes do Indico e Pacífico ocidental depreende-se do fato de se conhecerem 9 (mais
que 50%) das nossas espécies como ocorrentes das costas ocidentais do Oceano Indico
até ao Pacífico ocidental ou central. Aocorréncia, na Notogea, de uma Onchidella com
ramo renal recorrente ventral é estranha; a espécie tem estilete cuticular num
divertículo da bolsa penial, incomum no género.
MALACOLOGIA, 1965, 3(2): 263-286
1
SOME OPISTHOBRANCHIA FROM MICRONESIA
Ernst Marcus
Faculdade de Filosofia, Ciéncias e Letras
Universidade de Sao Paulo
Sao Paulo, Brasil
ABSTRACT
A Micronesian collection of 130 opisthobranchs belonging to the U. S. National
Museum contained 53 species.
less than 5 mm in length.
Only 10 of them are new, and half of these are
These small numbers show the uniformity of the
opisthobranch fauna on the reefs in the Indo-West Pacific Ocean, most of whose
bigger species are already known.
The following new species are described:
Stiliger (Ercolania) illus, Elysia bayeri, Elysia ratna, Hypselodoris cuis, Dis-
codoris lora,
Discodoris ylva, Catriona lonca, Catriona urquisa, Noumeaella
rehderi, and Muessa evelinae, the type-species of a new genus of the Favorini-
dae, allied to Herviella.
Some time ago, Dr. Harald A. Rehder
of the Smithsonian Institution, Washing-
ton, D.C., U.S.A., sent me for identifi-
cation a collection of 130 lots of opis-
thobranch mollusks from Micronesia.
All of this material was collected in
recent years by biologists and geolo-
gists sent out on surveys of islands in
several of the groups making up this
region of the central western Pacific.
Of the 53 species identified in this
sending, 10 are new, 5 of them being
less than 5 mm in length. The recog-
nized uniformity of the Indo-West Pacific
reef fauna, and the relatively advanced
state of exploration account for the small
percentage (18.9) of new species. Inour
first collection from the little known
coast of Brazil, 71.8% were new species.
My thanks are due to Dr. Harald A.
Rehder for having gone over the manu-
script, and to Dr. F. M. Bayer, of the
Marine Institute in Miami, Florida, for
having furnished many of the color notes
used inthe description of the new species.
SYSTEMATICS AND DISTRIBUTION
A systematic list of species of Euthy-
neura collected in Micronesia during the
field study are listed below. The species
are treated individually in consecutive
order in the section following the list.
Soleolifera, Onchidiacea, Onchidiidae
1. Peronia (Peronia) peronii (Cuv-
ier)
Cephalaspidea, Bullacea, Retusidae
2. Retusa sp.
Cephalaspidea, Philinacea, Phanero-
phthalmidae
3. Phanerophthalmus luteus (Quoy
and Gaimard)
Cephalaspidea, Philinacea, Aglajidae
4. Aglaja splendida Risbec
5. Chelidonura inornata Baba
6. Chelidonura hirundinina elegans
Bergh
Anaspidea, Aplysiidae, Aplysiinae
7. Aplysia (Varria) dactylomela
Rang
8. Aplysia (Varria) pulmonica Gould
9. Aplysia (Pruvotaplysia) parvula
Morch
Anaspidea, Aplysiidae, Dolabellinae
10. Dolabella auricularia (Solander)
Anaspidea, Aplysiidae, Dolabriferinae
11. Dolabrifera dolabrifera (Rang)
lPublished with the cooperation of the Institute of Malacology.
(263)
264
12. Petalifera
(Bergh)
Anaspidea, Aplysiidae, Notarchinae
13. Stylocheilus longicauda (Quoy and
Gaimard)
Sacoglossa, Elysiacea, Stiligeridae
14. Stiliger (Ercolania) illus, spec.
nov.
Sacoglossa, Elysiacea, Phyllobran-
chillidae
15. Phyllobranchillus
(Bergh)
16. Cyerce nigra Bergh
Sacoglossa, Elysiacea, Plakobranchi-
dae
17. Plakobranchus ocellatus van Has-
selt
Sacoglossa, Elysiacea, Elysiidae
18. Elysia thysanopoda Bergh
19. Elysia marginata (Pease)
20. Elysia bayeri spec. nov.
21. Elysia тата spec. nov.
Notaspidea, Pleurobranchacea,
Pleurobranchidae
22. Pleurobranchus peronii Cuvier
23. Pleurobranchus cf. lugubris
(Bergh)
24. Berthella grisea (Bergh)
25. Berthellina citrina (Rüppell and
Leuckart) i
Nudibranchia, Doridoidea, Crypto-
branchia, Hexabranchidae
26. Hexabranchus marginatus (Quoy
and Gaimard)
Nudibranchia, Doridoidea, Crypto-
branchia, Dorididae, Chromodoridinae
27. Chromodoris lineolata (van Has-
selt)
28. Chromodoris venusta (Bergh)
29. Hypselodoris cuis spec. nov.
30. Hallaxa decorata (Bergh)
Nudibranchia, Doridoidea, Crypto-
branchia, Dorididae, Miamirinae
31. Casella atromarginata (Cuvier)
32. Casella rufomarginata Bergh
Nudibranchia, Doridoidea, Crypto-
branchia, Dorididae, Discodorinae
33. Discodoris lora spec. nov.
34. Discodoris ylva spec. nov.
35. Kentrodoris funebris (Kelaart)
Nudibranchia, Doridoidea, Crypto-
branchia, Dorididae, Asteronotinae
petalifera pacifica
prasinus
E. MARCUS
36. Halgerda elegans Bergh
Nudibranchia, Doridoidea, Crypto-
branchia, Dorididae, Platydoridinae
37. Platydoris scabra (Cuvier)
38. Platydovis cruenta (Quoy and
Gaimard)
39. Platydoris cf. flammulata Bergh
Nudibranchia, Doridoidea, Phanero-
branchia, Nonsuctoria, Gymnodoridi-
dae :
40. Nembrotha nigerrima Bergh
Nudibranchia, Doridoidea, Porosto-
mata, Dendrodorididae
41. Dendrodoris nigra Stimpson
Nudibranchia, Doridoidea, Porosto-
mata, Phyllidiidae
42. Phyllidia (Phyllidia) varicosa
Lamarck
43. Phyllidia (Phyllidiella) pustulosa
Cuvier
44. Phyllidia (Phyllidiella) nobilis
(Bergh)
45. Fryeria rüppelli Bergh
Nudibranchia, Doridoidea, Dendro-
notoidea, Bornellidae
46. Bornella digitata (Adams and
Reeve)
Nudibranchia, Doridoidea, Dendrono-
toidea, Dotoidae
47. Doto cf. albida Baba
Nudibranchia, Doridoidea, Eolidoidea,
Acleioprocta, Cuthonidae
48. Catriona lonca spec. nov.
49. Catriona urquisa Spec. nov.
Nudibranchia, Doridoidea, Cleio-
procta, Favorinidae, Favorininae
50. Pteraeolidia semperi (Bergh)
51. Phyllodesmium hyalinum Ehren-
berg
52. Noumeaella rehderi spec. nov.
Muessa, (gen. nov.)
93. Muessa evelinae spec. nov.
Order Soleolifera
Superfamily Onchidiacea
Family Onchidiidae
1. Peronia (Peronia) peronii (Cuvier,
1804)
Mariana Islands: Saipan: from 1/2 ton
block of dead coral taken off anchor,
MICRONESIAN OPISTHOBRANCHIA 265
lagoon on west coast. Sta. loc. No. 2.
Е Ш Cloud, Jr., and J. .H.:O*Mara
coll, May 2, 1949. One specimen
(USNM 574622).2
Palau Islands: high tide line along
fringing reef on west shore of Abappao-
mogon Island (Ngermeiaus), about 1 1/2
miles west of Eil Malk, Sta. No. 260.
F. M. Bayer and R. R. Rofen coll.,
November 3, 1955. One specimen (USNM
575678).
Marshall Islands: Bikini Atoll: inter-
tidal. M. W. Johnson coll., April-May,
1946. Two specimens (USNM 574232).
Marshall Islands: Eniwetok Atoll:
Rujoru Id., on north outer side. Sta.
No. 4598. Jy Tracey: Jr; com
June 3, 1946. Two specimens (USNM
574235).
Marshall Islands: Eniwetok Atoll:
east side of south end of Eniwetok Id.
Sta. No. 4454. M. W. Johnson coll., May
20, 1946. One specimen (USNM 574234).
Marshall Islands: Eniwetok Atoll: on
exposed cobble’ rock flats, intertidal
zone, south ocean side at west end of
Igurin Id. Sta. No. 4472. J. P.E.
Morrison coll., May 22, 1946. One
specimen (USNM 574231).
Marshall Islands: Arno Atoll: reef
flat at Ine anchorage. Sta. No. 55.
J. W. Wells coll., June-August, 1950.
One specimen (USNM 574686).
Gilbert Islands: Onotoa Atoll: A. H.
Banner coll., August 15, 1951. One speci-
men (USNM 574925).
Order Cephalaspidea
Superfamily Bullacea
Family Retusidae
2. Retusa sp.
Marshall Islands: Bikini Atoll: under
coral head, outer reef, Bikini Island. Sta.
No. 65-1. F. M. Bayer coll., July 25,
1947. Color sketch made. Fragments of
one specimen (USNM 574440), in which
the absence of the radula was stated.
| 2U. $. National Museum Catalog Number.
Superfamily Philinacea
Family Phanerophthalmidae
3. Phanerophthalmus luteus (Quoy and
Gaimard, 1832)
Caroline Islands: Ifaluk Atoll: from
eel grass beds, south shore of lagoon,
Rauau district, north of Katelu benjo,
Falarik Id. Sta. No. 548. FM:
Bayer coll., October 8, 1953. Two
specimens (USNM 574970).
Family Aglajidae
4. Aglaja splendida Risbec, 1951
Palau Islands: Koror Island; in eel
grass in Geruherugairu Pass, between
Kaibakku Island and Kogai-hantó, Au-
luptagel Island. Sta. No. 30. F. M.
Bayer, coll., July 22, 1955. Black with
brilliant blue border. Two specimens
(USNM 575680).
5. Chelidonura inornata Baba, 1949
Caroline Islands: Ifaluk Atoll: la-
goon reef at Katelu benjo, near “Izzie”
and “Barbara” reefs, Rolong canoe
house. Sta. No. 724. F. M. Bayer,
coll., October 22, 1953. One specimen
(USNM 574979). Color: velvety black
with fine white flecks.
6. Chelidonura hirundinina elegans
Bergh, 1900
Marshall Islands: Bikini Atoll: creep-
ing on surface of rocks, outer reef
flats, Bikini Island. Sta. No.6. F.M.
Bayer, coll., August 5, 1947. Six speci-
mens (USNM 574439).
Order Anaspidea
Family Aplysiidae
Subfamily Aplysiinae
7. Aplysia (Varria) dactylomela Rang,
1828
Palau Islands: Urukthapel Island:
266 E. MARCUS
lagoon margin of reef on live coral and
coral rubble, with abundant Caulerpa and
Halimeda, north of east point(Nagareme-
diu). Sta. No. 69. Е. M. Bayer, coll.,
August 5, 1955. One specimen (USNM
575669).
Gilbert Islands: Onotoa Atoll: from
green algal veneers on dead coral rock,
NW corner of atoll. Sta. No. GOC-41.
P. E. Cloud, coll., August 21, 1951.
Two specimens (USNM 575058), identi-
fied by Dr. N. B. Eales.
8. Aplysia (Varria) pulmonica Gould,
1852
Marshall Islands:
lagoon reef south of causeway be-
tween Lidilbut and Elangelap Islands.
Sta. No. 1514. H.S. Ladd, M. Russell,
and R. C. Townsend coll., May 11,
1952. One specimen (USNM 574922),
identified by Dr. N. B. Eales as prob-
ably representing this species.
9. Aplysia (Pruvotaplysia) parvula
Mörch, 1863
Gilbert Islands: Onotoa: on algae,
ocean side of reef flat. E. Moul, coll.,
August 6, 1951. The single specimen
(USNM 575371) collected represents
the variety nigrocincta von Martens,
1880.
Subfamily Dolabellinae
10. Dolabella auricularia (Solander,1786)
Mariana Islands: Guam: J.L. Gres-
sitt, coll., October, 1945. One specimen
(USNM 574206).
Palau Islands: Iwayama Bay: shallow
area in Geruherugairu Pass between
Kaibakku Island and Kogai-hentó, Aulu-
ptagel Island; in 5-6 feet on coral and
sand bottom with eel grass, Halimeda
and Padina. Sta. No. 85. Е. М. Bayer
et al. coll., August 12, 1955. Two speci-
mens (USNM 575683). |
Palau Islands: same as above, in 4-5
feet. Sta. No. 140. Е. M. Bayer et al.
Eniwetok Atoll:
coll., August 30, 1955. Two specimens
(USNM 575713).
Caroline Islands: Kapingamarangi
Atoll: lagoon reef, Hare Island Sta.
No. 291. C. Hand coll., July 20, 1954.
One specimen (USNM 575712).
Dr. Harald A. Rehder called my
attention to the fact that the name
Dolabella scapula Martyn, 1784,
by which this species has gener-
ally been known, is invalid, since
Martyn’s work “The Universal Con-
chologist” has been rejected for
nomenclatorial purposes by the
International Commission on Zoolo-
gical Nomenclature (Opinion 456-
1956).
Subfamily Dolabriferinae
11. Dolabrifera dolabrifera (Rang, 1828)
Palau Islands: reef flat on outer
barrier reef, about 2 miles SSW of
Ngaremediu District, east of Urukthapel
Island. Sta. No. 111. F. M. Bayer et al.
coll., August 19, 1955. Two specimens
in about 1 foot on alga-encrusted coral
rock (USNM 575684).
Caroline Islands: Ifaluk Atoll: sea-
ward reef at Fan-ni-wa canoe-house
trail, middle of Falarik Island. Sta. No.
443. F. M. Bayer coll., October 1, 1953.
Two specimens (USNM 574966 and
574967).
Caroline Islands: Ifaluk Atoll: on
rocks in sand flats, lagoon side, at south
end of Falarik Island. Sta. No. 738. F.
M. Bayer coll., October 26, 1953. Two
specimens (USNM 574981).
Caroline Islands: Kapingamarangi
Atoll: on rock pile, lagoon, Hare Island,
Sta. No. 604. C. Hand coll., August
6, 1954. Three specimens (USNM
575689).
Caroline Islands: Kapingamarangi
Atoll: inner reef flat, Touhou Island.
Sta. No.67. C. Hand coll., June 25, 1954.
One specimen (USNM 575690).
Marshall Islands: Bikini Atoll: Inner
reef under rocks, Bikini Island. Sta. No.
278. F. M. Bayer coll., August 24,
MICRONESIAN OPISTHOBRANCHIA 267
1947. Two specimens (USNM 574441).
Gilbert Islands: Onotoa Atoll: in two
feet, tide pool, Heliopora reef flat. A.
H. Banner coll., August 1, 1951. Two
specimens (USNM 575374).
12. Petalifera petalifera pacifica
(Bergh, 1900)
Caroline Islands: Ifaluk Atoll: from
eel grass, south lagoon shore, Rauau
district, N of Katelu benjo. Sta. No.
549. Е. М. Bayer coll., October 8,
1953. Ten specimens (USNM 574972
and 574969).
Subfamily Notarchinae
13. Stylocheilus longicauda (Quoy and
Gaimard, 1825)
Caroline Islands: Ifaluk Atoll: north
end, Transect C, Falarik Island. Sta.
No. 446. F. M. Bayer coll. One speci-
men and one radula slide (USNM 574968).
Caroline Islands: Ifaluk Atoll: from
eel grass beds, south lagoon shore,
Rauau district, north of Katelu benjo.
Sta. No. 548 and 549. F. M. Bayer
coll., October 8, 1953. Two specimens
(USNM 574971 and 574974).
Caroline Islands: Ulithi Atoll: Asor
Island. Stars No. il. Fi Ne? Young
coll., May, 1945. One specimen (USNM
574471).
Marshall Islands: Bikini Atoll: boat
- Cradle anchored off Bikini Island. Sta.
No. 4. Е. М. Bayer and Е. С. Zimmer-
man coll. August 28, 1947. Four speci-
mens (USNM 574437).
Order Sacoglossa
Superfamily Elysiacea
Family Stiligeridae
14. Stiliger (Ercolania) illus, spec. nov.
(figs. 1-4)
Material: Caroline Islands: Ifaluk
Atoll: on large flabellate alga, lagoon
reef south of Elangelap, western rim of
atoll. Sta. No. 41. R. R. Rofen coll.,
October 10, 1953. One specimen.
Description: Length 2.5 mm, dark
brown with light tips of cerata. Head
with big black eyes close together in
front between rhinophores. These flat-
tened on outside, with an auriculate lobe
at basal third, similar to Ercolania
pancerii Trinchese (Vayssiére, 1888:
126, pl. 6,f. 108). No labial tentacles.
Foot anteriorly rounded, without elon-
gated corners. Cerata in irregular
rows, leaving middle of back free, total
number 21, several having fallen off;
largest cerata medial, smaller ones
lateral. Base of cerata narrow, tip
mamillary, middle swollen and almost
knobbed due to racemose diverticula of
digestive gland. No branches of albumen
gland in cerata. Long penis (0.45 mm),
completely retracted into male atrium;
no stylet.
Radula consisting of 8 teeth in ascen-
ding, 7 in descending limb, several in
ascus. Total length of tooth 54 y, incl.
20 y long base; cusp a slender lowblade,
its height in the middle (7.5 п) gradually
tapering towards the tip; cutting edge
smooth.
Holotype: the slug and one slide with
radula and penis (USNM 574960).
Discussion: The generic position of
the present species is Somewhat doubt-
ful. The absence of a penial stylet
seems certain and can hardly be con-
sidered tohave been torn off after mating,
as has been observed in St. (St.) vossi
Marcus (1960a: 146) whose copulatory
organ was found everted in the 3 ex-
amined slugs. The diameter and posi-
tion of the eyes suggest Costasiella Pru-
vot-Fol (1951a: 73), but the type-species
has tentacle-like projections at the
angles of the foot, and these are also
somewhat elongated in C. ocellifera
(Simroth, 1895: 168) and C. nonatoi
Marcus (1960a: f. 26). The cerata of
the latter, the only anatomically known
Costasiella, contain branches of the al-
bumen gland along with those of the di-
gestive gland.
The surveys of Ercolania (Pruvot-
Fol, 1954a: 191; Marcus, 1956: 7; Baba,
MICRONESIAN OPISTHOBRANCHIA 269
1959: 327) include 3 more or less dark
species: E. trinchesei Pruvot-Fol
(1951a: 71) with bright yellow basal half
of the cerata, E. akkeshiensis Baba
(1935: 116) whose radular teeth are
high, not tapering toward the tip, and E.
noto Baba (1959: 330) with broad labial
tentacles.
I maintain Ercolania Trinchese, 1872,
as a subgenus of Stiliger Ehrenberg,
1831 (Marcus, 1956: 6).
Family Phyllobranchillidae
Genus Phyllobranchillus Pruvot-Fol,
1933
In a recent paper (Marcus and Mar-
cus, 1963, p. 17) we used Polybranchia
Pease, 1860. Because, however, thetype
species P. pellucida Pease is a “species
inquirenda” we now consider Pease’s
genus as a doubtful one.
FIGS. 1-4. Stiliger (Ercolania) illus, sp. n.
Two radular teeth. FIG. 4. Penis.
15. Phyllobranchillus prasinus (Bergh,
1871)
Caroline Islands: Ifaluk Atoll: on
coral rocks on sand flats, lagoon side
of south end, Falarik Island. Sta. No.
735. РЕ. М. Bayer coll., October 26,
1953. One specimen and radula slide
(USNM 574980).
P. orientalis Kelaart, 1858, may be
the same species.
16. Cyerce nigra Bergh, 1871
Caroline Islands: Ifaluk Atoll: from
algae in 6 feet, sandy bottom, lagoon
shelf near margin of the west reef,
between Elangelap and Falarik Islands.
Sta. No. 138-E-3. D. P. Abbott coll.,
October 20, 1953. One specimen (USNM
575700).
Caroline Islands: Ifaluk Atoll: from
FIG. 1. Dorsal view. FIG. 2. Ceras. FIG. 3.
‚ FIGS. 5-6. Elysia bayeri, sp.n. FIG. 5. A. Creeping slug from a drawing by Dr. F. М. Bayer.
B. Slug with opened parapodia from a painting by Dr. F. M. Bayer. FIG. 6. Radular tooth.
FIGS. 7-8. Elysia ratna, sp. n. FIG. 7. Dorsal view. FIG. 8. Radular tooth.
FIGS. 9-13. Hypselodoris cuis, sp. n.
armature near margin;
FIG. 9. Dorsal view.
left side, surface focussed;
FIG. 10. Elements of labial
right side, bottom focussed. FIG. 11.
Labial armature near centre. FIG. 12. One labial platelet, side view. FIG. 13. Radular teeth.
Three innermost and one 2nd tooth; one from middle of row; one outermost.
FIGS. 14-17. Discodoris lora, sp. n.
FIG. 14. Dorsal view.
FIG. 15. Sculpture of notum.
FIG. 16. Rodlet of labial cuticle. FIG. 17. One radular tooth from middle ofrow and the 2 outer-
most teeth.
Abbreviations used in Figs. 1-41
а - ampulla
am - common atrium
ar - anus
с - spermatocyst
ce - base of plucked ceras
d - ejaculatory duct
e - sheathed part of efferent duct
eu - female duct
f - female gland mass
g - genital aperture
h - hermaphrodite duct
ma - male atrium
ne - cnidosac
ni - nidamental duct
oi - inner oviduct
p - penis
q - prostate
s - spermatheca
se - efferent duct
so - spermoviduct
sr - sphincter
u - fertilizing (uterine) duct
у - vagina
270 E. MARCUS
algae in 12 feet, sandy bottom lagoon
shelf, north of center of Ella (=Elange-
lap) Island. Sta. No. 158-159. R. R. Ro-
fen and Yaniseiman coll., October 24,
1953. Two specimens (USNM 575699).
Family Plakobranchidae
17. Plakobranchus ocellatus van
Hasselt, 1824
Palau Islands: on alga-encrusted
coral rocks, reef flat on outer barrier
reef about 2 miles SSW of Ngaremediu
District, east of Urukthapel Island. Sta.
No. 111. F. M. Bayeretal.coll., August
19, 1955. One specimen and radula
slide (USNM 575662).
Family Elysiidae
18. Elysia thysanopoda Bergh, 1905
Palau Islands: in 2-3 1/2 feet, coral
and sand bottom, with eel grass, Hali-
meda and Padina, shallow area in
Geruherugairu Pass, between Kaibakku
Island and Kogai-hantô, Auluptagel
Island. Sta. No. 85А. Е.М. Bayer et al.
coll., August 12, 1955. Two specimens
(USNM 575674). |
19. Elysia marginata (Pease, 1871)
Palau Islands: in 3-10 feet, fringing
reef on west shore of Abappaomogon
Island (Ngermeiaus) about 1 1/2 miles
west of Eil Malk. Sta. No. 260. F. M.
Bayer and R.R. Rofen coll., November 3,
1955. Three specimens (USNM 575677).
Marshall Islands: Bikini Atoll: on
alga-covered rocks, lagoon reef of Bikini
Island. Sta. No. 278. F. M.Bayer coll.,
August 24, 1947. Five specimens and
radula slide (USNM 574442).
20. Elysia bayeri spec. nov.
(Figs. 5-6)
Material: Marshall Islands: Bikini
Atoll: outer reef, Bikini Island. Sta.
No. 65B. F. M. Bayer coll., July 29,
1947. One specimen.
Description: Living slug 12 mm long.
According to Dr. Bayer’s painting, back
of head, rhinophores and pericardial
eminence with black and white stripes,
tips of rhinophores orange with white
stripes. Two longish blue spots in mid-
line of head and neck. Dorsal surface
dark green, outwards a band of lighter
green, followed by a broad black and a
broad bright orange margin. Under
surface of parapodial border with
blackish brown blotches alternating with
light orange. Ventral side black with
longitudinal narrow white stripes; near
parapodial border broad blue dashes,
corresponding to orange portions of
brim.
Preserved specimen 6 mm long, 4mm
broad. Back of head and body black
except white edging of rhinophores, para-
podia and anus; latter situated between
mid-line and front edge of right para-
podium. Ventral surface light; border
of parapodia with black blotches alter-
nating with light intervals and running
out into gray triangles towards foot.
Radula comprising about 15 free teeth
and several in ascus. Base and cusp
each 25 yu long, tip of cusp a curved
point; cutting edge with 15 blunt denti-
cles; groove on outer surface long,
shallow.
Named for Dr. Frederick M. Bayer.
Holotype: slug and radula slide (USNM
574438).
Discussion: The color, not quite un-
like that of E. ornata (Pease, 1860; see
Bergh, 1905: 84), characterizes the
species well. Also the nature of the
radular tooth is uncommon in Elysia,
though not unique, as E. livida Baba
(1955: f. 13) has a similar tooth.
21. Elysia ratna spec. nov.
(Figs. 7-8)
Material: Palau Islands: Iwayama
Bay: in 0-10 feet, in cave formed by
west arm of Kogai-hantó, Auluptagelld.,
near islets XXXII and XXXIV. Sta. No.
47. F. M. Bayer et al. coll., July 28,
MICRONESIAN OPISTHOBRANCHI 271
1955. One specimen.
Description: Length 14 mm, breadth
8 mm. Head covered by rhinophores,
these black on sides, light, in pre-
served specimen cream, in middle.
From black margins several spike-like
pigmented stripes project towards light
area, subdividing it. Dorsal side ofbody
and parapodia black with light, now
yellowish margin. Pericardial eminence
with light longitudinal stripes. Ventral
side with light and dark longitudinal
stripes, these more numerous and darker
on sole than on underside of parapodia.
Foot with light borders, concave in front.
Radula containing 20 free teeth and about
Same number in ascus. Base 22, cusp
28 u long, tip hooked, cutting edge with
about 18 pointed denticles; furrow on
outer surface deep.
Holotype: slug andradula slide (USNM
575705).
Discussion: Inthe discussion of Elysia
latipes (Marcus,1960b: 899) the literature
of the Indo-west-pacific species of Elysza
was brought together. The new species
differs from all those described in these
papers by the great extent of black pig-
ment, quite rare in Elysia. Furthermore,
in the markedly dark forms of Bergh
(1905: 85-87) the color is not arranged
as it is in Е. тата. The stripes on
rhinophores, pericardial eminence and
underside are similar to those of E.
bayeri, but the shape of the radular tooth
is very different.
Order Notaspidea
Superfamily Pleurobranchacea
Family Pleurobranchidae
22. Pleurobranchus peronii Cuvier,
1804 (Vayssiére, 1898, emend.)
Palau Islands: in 0-4 feet on lagoon
margin of reef, north of east point
(Ngaremediu) of Urukthapel Island. Sta.
No. 69. F. M. Bayer et al. coll.,
August 8, 1955. Two specimens and
Slide with radula and jaws (USNM
575667).
Oscaniella
purpurea Bergh, 1897,
1905, is a synonym.
23. Pleurobranchus cf. lugubris
(Bergh, 1905)
Palau Islands: Iwayama Bay: in 3-20
feet on coral shelf along west shore of
SE peninsula of Koror Island, at mouth
of Kaki Suidó (Oyster Pass). Sta. No.
236. H. A. Fehlman, S. Pierce, R. R.
Rofen coll. One specimen and slide
with radula and jaws (USNM 575670).
Palau Islands: Iwayama Bay: in 0-
3 feet, eel-grass, sand, and coral flat
in Geruherugairu-suido, between Kai-
bakku Island, and Kogai-hantô of
Auluptagel Island. Sta. No. 30. Е. М.
Bayer et al. coll., July 22, 1955. One
specimen (USNM 575681).
24. Berthella grisea (Bergh, 1905)
Palau Islands: Iwayama Bay: 0-15
feet, “Bay of the Dragon Palace,”west
side of Kogai Peninsula, Auluptagel
Island, between USA and Tai Islands.
Sta. No. 100. F. M. Bayer etal. coll.,
August 16, 1955. One specimen and slide
with radula and jaws (USNM 575676).
25. Berthellina citrina (Rüppell and
Leuckart, 1828)
Palau Islands: in 0-1 feet onreefflat,
on outer barrier reef, about 2 milesSSW
of Ngaremediu district, east of
Urukthapel Island. Sta. No. 111. Е. М.
Bayer et al. coll., August 19, 1955. One
specimen and slide with radula and jaws
(USNM 575664).
Order Nudibranchia
Suborder Doridoidea
Infraorder Cryptobranchia
Family Hexabranchidae
26. Hexabranchus marginatus (Quoy
and Gaimard, 1832)
Caroline Islands: Ifaluk Atoll: lagoon
shore, Rauau, Falarik Island (taken from
Golden Plover). Sta. No. 593. F. M.
272 E. MARCUS
Bayer coll., October 15, 1953. One
specimen and slide with radula and jaws
(USNM 574975).
Marshall Islands: Eniwetok Atoll:
north of Rigoru Island. Sta. No. 4592.
J. P. E. Morrison coll., June 2, 1946.
One specimen (USNM 57422).
Family Dorididae
Subfamily Chromodoridinae
27. Chromodoris lineolata (van
Hasselt, 1824)
Palau Islands: Iwayama Bay: on eel
grass, sand and coral flat in
Geruherugairu Pass, between Kaibakku
Id. and Kogai-hantó, Auluptagel Id. Sta.
No. 30, F. M. Bayer et al. coll., July
22, 1955. One specimen (USNM 575679).
Palau Islands: Iwayama Bay: on eel
grass, sand and coral flat in Geruheru-
gairu Pass, between Kaibakku Id. and
Kogai-hantó, Auluptagel Id. Sta. No. 85A.
Е. M. Bayer et al. coll., August 12, 1955.
One specimen (USNM 575675).
Palau Islands: Iwayama Bay: Sandy
flat and fringing reef at south end of
Gua-zima (Island XV); Abe’s traverse
XIII. Sta. No. 92. Е. M. Bayer et al.
coll., August 14, 1955. One specimen
(USNM 575666).
Palau Islands: Koror Island: in
Madalai District, extreme west end of
Koror Island, shore at S end of
Arakabesan-Madalai causeway, man-
grove shore grading into mud and sand
flat. Sta. No. 12. F. M. Bayer etal.
coll., July 9, 1955. One specimen (USNM
575685): black with longitudinal lines,
anastomosing here and there; margins
of mantle sepia; branchial plumes sepia
with white flecks; rhinophores dark
sepia with white flecks; sole of foot
grayish; tips of tentacles brownish
yellow.
28. Chromodoris cf. venusta Bergh,
1905
Palau Islands: Iwayama Bay: east side
of mouth of Kaki-suidö (Oyster Pass),
between Island XXIX and SE endof Koror
Id. Sta. No. 220A. Е. М. Bayer et al.
coll., October 12, 1955. One specimen
and slide of radula and jaws. (USNM
575702).
29. Hypselodoris cuis, spec. nov.
(Figs. 9-13)
Material: Caroline Islands: Kapinga-
marangi Atoll: Polim reef flat, near
Tipongowarakam Pass, Greenwich (Ship)
Pass. Sta. No. 723. С. Hand сова
August 12, 1954. One specimen.
Description: Length 6.5, breadth 3,
height 3.5 mm. Light brownish with
lighter opaque knots, which are subepi-
dermal, longish, more or less sym-
metrically disposed in about 10 rows on
notum and hyponotum. Skin smooth;
brim of notum hardly salient. Tentacles
grooved on outer side. Rhinophores
nearer to border than to one another.
Nine unipinnate gills. Foot narrower
than notum; anterior border bilabiate,
not notched in middle; tail projecting
behind.
Labial cuticle forming two triangular
areas of pleurobranchid-like platelets.
Their prolonged either simple or split
tips (Figs. 10-12) lie like scales over
bases of following platelets. Radula with
52 rows of 35.0.35 teeth; no rhachidian
thickening. Teeth with two principal
cusps. Innermost tooth with 2 denticles
on inner and 3 on outer side; following
teeth with 3-5 denticles, only on outer
side and number decreasing outwards.
Holotype: slug and slide of radula and
labial armature (USNM 575708).
Discussion: As recently exposed
(Marcus, 1960b: 901), I follow Odhner
(1957) in suppressing Glossodoris
Ehrenberg, 1831, and using Chromo-
doris Alder and Hancock, 1855, for
species with unicuspidate teeth, Hypselo-
doris Stimpson, 1855, for those with
bicuspidate ones.
While the labial armature of this sub-
family generally consists of rodlets,
straight or ending with a bifid hook, a
number of species of Hypselodoris have
MICRONESIAN OPISTHOBRANCHIA
scale-like platelets as labial elements.
According to Basedow and Hedley (1905:
141) Bergh’s first Chromodoris crossei
(1884: 648) is identical with the type-
species of Hypselodoris, Goniodoris ?
obscura Stimpson (1855: 388-389). Hence
simple labial hooklets combined withbi-
cuspidate teeth (Bergh, 1883: pl. 7, 8)
occur in the type-species. H. runcin-
ata (Bergh, 1877: 479) and H. maren-
zelleri (Bergh, 1882: 219) are further
examples.
Some species of Hypselodoris with
platelets are: H. crossei (Angas, 1864;
Bergh, 1905: 146), H. semperi (Bergh,
1877: 482; 1905: 147), H.hilaris (Bergh,
1890: 935; Baba 1953: 210), H. nigro-
striata (Eliot, 1904: 394; 1905: 247),
H. tenuilinearis (Farran, 1905: 342;
Eliot, 1905: 246, 248), and H. ransoni
(Pruvot-Fol, 1954b: 18). Though some
of these species are evidently identical
with one another (Eliot, 1. c.; Pruvot-
Fol, 1951b), the labial armature should
not be disregarded; a list of synonyms
as that given by Risbec (1953: 66) for
H. diardii cannot be accepted.
Н. cuis comes closest to H. ransoni
from French Oceania and especially to
H. hilaris from Amboina and the Kii
Peninsula. NH. тапзот has less outer
denticles on the middle teeth than cuis,
and its marginal teeth have no cusps.
Moreover the labial armature of H.
vansoni consists of four separate
areas. The specimen of H. hilavis from
Amboina has narrower labial platelets
than cuis; in the variety from Middle
Japan they do not differ, nor does the
radula, but the back has 5 longitudinal
bright purple lines which can hardly be
assumed to have faded out into light
knots.
30. Hallaxa decorata (Bergh, 1878)
Caroline Islands: Kapingamarangi
Atoll: Polim reef flat, near Tipongo-
wasakam Pass in Greenwich (ship) Pass.
Sta. No. 722. C. Hand coll., August
12, 1954. One specimen and slide with
radula and jaws (USNM 575694).
273
Subfamily Miamirinae
31. Casella atromarginata (Cuvier,
1804)
Marshall Islands: Bikini Atoll: in 28
fms., 4 miles south of west end of Bikini
Id. Sta. No. R4356. J. P. E. Morrison
coll., April 25, 1946. One specimen
and slide with radula and jaws (USNM
574227).
32. Casella rufomarginata Bergh,
1890
Palau Islands: in shallow water on
reef flat on outer barrier reef about
2 miles SSW of Ngaremediu District,
east of Urukthapel Island. Sta. No. 111.
F. M. Bayer et al. coll., August 19,
1955. One specimen and slide with
radula and jaws (USNM 575673).
Palau Islands: on reef flat, Ngadarak
Reef, north of mouth of Malakal pass.
Sta. No. 106. F. M. Bayer et al. coll.,
August 17, 1955. One specimen and
slide with radula and jaws (USNM
575672).
Subfamily Discodorinae
33. Discodoris lora spec. nov.
(Figs. 14-18)
Material: Caroline Islands: Ifaluk
Atoll: washed from algae, algal edge
exposed at low tide, reef east of south
end of Falarik islet, just north of Tran-
sect A. Sta. No. 26. D. P. Abbott coll.,
September 4, 1953. One specimen.
Description: Length 12 mm, breadth
6.5 mm, height 3 mm, hence rather
flat. Yellowish with black dots on
notum, concentrated around the larger
of the numerous round, unequal warts.
Spicules not found. Tentacles rather
large, outer side grooved; rhinophores
less distant from borders than from one
another; rim of their pockets smooth;
clubs with about 12 leaves. Six tri-
pinnate gills; rim of their pocket
smooth; anal region bulged out in the
E. MARCUS
274
MICRONESIAN OPISTHOBRANCHIA 275
preserved specimen, possibly thereby
anus removed from centre. Hyponotum
smooth, its transverse striation due to
muscle fibres showing through epi-
dermis. Foot nearly 4 mm broad, an-
terior border withtransverse groove and
median notch of upper lip; hind end
round, not projecting beyond notum.
Labial cuticle yellow with up to 80,
high, 12-15 „ thick rodlets, consisting
of superposed discs. Pharynxbig, 4 mm
long. Radula narrow, long, pro-
jecting beyond hind end of pharyngeal
bulb; 50 rows of 12.0.12 teeth. These
hamate, smooth; innermost tooth 60 u
high, teeth in the middle 120 y, outer-
most tooth shortest, 50 y. The latter
with long base and short cusp.
Hermaphrodite duct (h) dilated into
sausage-shaped ampulla (a) whose out-
let coincides with separation of male and
female ducts. Efferent duct begins with
voluminous prostate (q), continues (d)
with simple musculature, followed by
ciliate part surrounded by special mus-
cle sheath (e), ending with pleurembolic
penis (p), “glans” of Bergh’s termino-
logy, in male atrium (m) or “prae-
putium”. Narrow vagina (v) between
latter and nidamental duct (ni), leading
to spermatheca (s). Uterine duct (u)
begins immediately beside entrance of
vagina. Spermatocyst (c) intercalary in
uterine duct which enters female gland
mass (f) far in front.
Holotype: Slug and slide with radula
and labial rodlets (USNM 575709).
Discussion: The majority of the
about 40 species of Discodoris is known
from the Indo-West Pacific Ocean. Only
the following 6 species with a similar
narrow radula must be compared with
D. lora. D. indecora Bergh, 1881,
from the Mediterranean Sea and the Cape
Verde Islands is olivaceous with light
dots, and its rhinophores have 15-20
perfoliations. D. dubia Bergh, 1904,
dubia var., and D. egena Bergh, 1904,
all from the NW coast of Tasmania,
differ from D. lora by shape of the outer-
most radular tooth and number of rhino-
phorial leaves. D. egena is generically
uncertain, as a prostate could not be
found. The geographically closest Dis-
codoris with narrow radula, D. liturata
Bergh, 1905, N of Sumbawa, has black
notum with few white blots, transversely
striped notal margin set off from centre,
and distally curved labial rodlets. D.
pallida Baba, 1937, from the W coast
of Kyushu, has 9 gills and 15 radular
rows. The geographically far distant
D. erythraeensis Vayssiére, 1912, from
the Red Sea, is morphologically nearest
to D. lora, but differs by its upright
outermost radular tooth, whose base is
quite short, and by black spots also on
the sole.
34. Discodoris ylva spec. nov. (Figs.
19-22)
Material: Gilbert Islands: Onota
Atoll: tide pool on Нейорота flat, 60 cm
deep. A. H. Banner coll., August 1,
1951. One specimen.
Description: Length 11 mm, breadth
8 mm, rather flat. Yellowish, sprinkled
with fine black dots on notum, concen-
trated in many bigger spots. Back with
caryophyllidia which contain pigment
Specks, are bigger in middle, smaller
towards borders. Spicules numerous,
thin,. some of them stand out from tip
of caryophyllidia. Border of notum in-
complete, probably due toautotomy. Hy-
FIG. 18. Discodoris lora, sp. n. Diagram of reproductive organs, from dissection.
FIGS. 19-22. Discodoris ylva, sp. n.
productive organs, from dissection.
FIGS. 23-26. Catriona lonca, sp. n.
FIG. 19. Dorsal view.
and from above. FIG. 21. Innermost and 5 outermost teeth of radula.
FIG. 20. Tentacle from below
FIG. 22. Diagram of re-
FIG. 23. Right side view. FIG. 24. Jaw and denticles
of masticatory process. FIG. 25. Radular tooth. FIG. 26. Penial stylet.
FIGS. 27-30. Catriona urquisa, sp. п. FIG. 27. Right side view. FIG. 28. Jaw and denticles
of masticatory process. FIG. 29. Smallest radular tooth. FIG. 30. Middle-sized radular tooth.
FIG. 31. Noumeaella rehderi, sp. п. Left rhinophore.
276 E. MARCUS
ponotum spiculate, transparent, showing
spicules forming spikes around bases of
caryophyllidia.
Tentacles hidden in concavity in front
of fore end of foot, triangular with outer
side thrown into 5 or 6 transverse folds.
Rhinophores about as far from one ano-
ther as from edges of notum, clubs with
14 leaves. Rim of rhinophorial pocket
bordered with caryophyllidia. So is
border of gill-cavity which is empty;
gills probably bitten off. Anterior bor-
der of foot transversely grooved, upper
lip notched; hind end of foot damaged.
Labial cuticle with two areas of yellow-
ish, stratified 50 » high rodlets. Radula
with 21 rows and 30 teeth on either side
of rhachis. Length of teeth, in micra:
innermost 34, in middle 120, 26th to
30th 90, 80, 70, 60, 50: Most teeth
simple hooks, of the outermost ones
most frequently 2, exceptionally 1 or 3,
with 1-5, generally 1 or 2, accessory
cusps. Base of outermost tooth short.
Hermaphrodite duct (в) widens to form
slender ampulla (a) whose outlet divides
into male and female (oi) ducts. Male
duct merges into massive white prostate
(q). Following tubular duct first brown
and glandular, then white, muscular (d).
Soft pleurembolic penis (p) hangs into
male atrium. Vagina (v) begins broad,
narrows internally. Spermatheca (s)
contains brownish masses. Uterine duct
goes out from vagina, leads to sperma-
tocyst (c) filled with silky white orien-
tated sperm and is connected with female
gland mass (f) by short insemination
duct (u).
Holotype: Slug and two slides, one
with radula and labial rodlets, and one
with genital ducts (USNM 575377).
Discussion: The peculiar oral tenta-
cles resemble those of Tyrinna Bergh,
1898, a widely distant genus related with
Cadlina (Marcus, 1959: 29). Digitiform
tentacles are common in Discodoris
(Eliot, 1903: 553). If these are long and
conspicuous as in D, palma Allan (1933:
448) from Pussy-cat Bay near Sydney,
they might contract in such a way that
outer folds are brought about. However,
in the descriptions of preserved speci-
mens of numerous species of Discodoris
transversely folded tentacles were never
mentioned.
In the type-species of the genus, D,
boholiensis Berg (1877: 519) and the 7
other species published together with it
the cusps of all teeth are simple hooks.
Species whose outer teeth have split
cusps are D, erubescens Bergh (1884:
662), D. lutescens Bergh (1905: 103;
misprint in title line), and D. pallida
Baba (1937: 305). Together with D. ylva
they could possibly constitute an own
taxon and reduce the genus Discodoris
which is difficult to follow in the present
state. But the occurrence of split
cusps is not sufficiently constant (Baba,
1937: 306) for a clear cut differentiating
character. Onthe other hand this charac-
ter cannot be neglected, and the other-
wise similar D. labifera (Abraham, 1877;
Farran, 1905: 335) must be held apart
from D. ylva by reason of the simple
hooks of its radular teeth.
D. erubescens has pointed villi on the
notum, D. lutescens tuberculiform tenta-
cles, and D. pallida 14-17 teeth in the
half-row of the radula.
35. Kentrodoris funebris (Kelaart, 1859)
Palau Islands: Iwayama Bay: sandy
flat and fringing reef at south end of
Gua-zima (Island XV), Abe’s Traverse
XIII. Sta. No. 92. Е. M. Bayer et al.
coll., August 14, 1955. Two specimens
and one radula slide (USNM 575665).
Caroline Islands: Kapingamarangi
Atoll: Lagoon reef, Hare Island Sta. No.
606, C. Hand coll., August 6, 1954.
One specimen (USNM 575686).
Caroline Islands: Kapingamarangi
Atoll: Thokataman Is., poisoned along
with fish by rotenone. C. Hand coll.,
July 12, 1953. One specimen (USNM
575687).
K. annuligera Bergh,
synonym.
1876, is a
Subfamily Asteronotinae
36. Halgerda elegans Bergh, 1905
Marshall Islands: Rongelap Atoll:
lagoon. Lt. Kaley coll., June 20, 1946.
|:
5
MICRONESIAN OPISTHOBRANCHIA
One specimen and radula slide (USNM
574165). Color: deep purple with white
ring-like markings.
Subfamily Platydoridinae
37. Platydoris scabra (Cuvier, 1804)
Caroline Islands: Kapingamarangi
Atoll: lagoon reef under coral boulder,
Tiatua Id. Sta. No. 157. C. Hand coll.,
July 13, 1954. One specimen and slide
of radula and labial cuticle (USNM
575693).
Marshall Islands: Bikini Atoll: south
half of Enyu Island. Sta. No. R 4028.
J. P. E. Morrison coll., March 5, 1946.
One specimen (USNM 574228).
38. Platydoris cruenta (Quoy and
Gaimard, 1832)
Mariana Islands: Guam. J. L. Gres-
sitt coll., October, 1945. One specimen
and slide with radula and labial cuticle
(USNM 574207).
Caroline Islands: Ifaluk Atoll: under
rocks middle of reef flat, north end of
Transect C. Falarik Id. Sta. No. 439.
F. M. Bayer coll., October 1, 1953. Two
specimens and slide with radula and
labial cuticle (USNM 574965).
Caroline Islands: Ifaluk Atoll: from
rocks and boulders of elang, south end
of Falarik Id. Sta. No. 799. F. M.
Bayer coll., October 31, 1953. One
specimen (USNM 574983).
Gilbert Islands: Onotoa Atoll: in
tide pool, 1 foot deep, on Heliopora flat.
A. H. Banner coll., August 1, 1951.
One specimen (USNM 575373).
39. Platydoris cf. flammulata Bergh,
1905
Caroline Islands: Ifaluk Atoll: from
beneath boulders, outer elang of Elange-
lap Id. Sta. No. 351. F. M. Bayer coll.,
September 20, 1953. One specimen
(USNM 574961).
Infraorder Phanerobranchia
277
Superfamily Nonsuctoria
Family Gymnodorididae
40. Nembrotha nigerrima Bergh, 1877
Palau Islands: reef flat of Ngada-
rak Reef, north of mouth of Malakal
pass. Sta. No. 106. F. M. Bayer etal.
coll., August 17, 1955. One specimen
and slide with radula and labial cuticle
(USNM 575671).
Palau Islands: lagoon margin of reef,
north of east point(Ngaremediu)of Uruk-
thapel Id. Sta. No. 69. F.M. Bayer
et al. coll., August 8, 1955. Two speci-
mens (USNM 575668).
Infraorder Porostomata
Family Dendrodorididae
41. Dendrodoris nigra (Stimpson, 1855)
Gilbert Islands: Onotoa Atoll: Sta.
АТ-Ш. D. W. Strasburg coll., July 16,
1951. One specimen (USNM 575369).
Gilbert Islands: Onotoa Atoll: reef
flat, ocean side. J. E. Randall coll.,
September 9, 1951. One specimen (USNM
575370).
Gilbert Islands: Onotoa Atoll: Sta.
No. A-5. А. H. Banner coll., July 25,
1951: One specimen (USNM 575376).
Family Phyllidiidae
42. Phyllidia (Phyllidia) varicosa
Lamarck, 1801
Mariana Islands: Saipan: lagoon west
side of Saipan. Sta. No. c-7-a. P.E.
Cloud, Jr. coll., April 10, 1949. One
specimen (USNM 574620).
Mariana Islands: Guam: Oca Point.
Sta. №. 102 :(255) .(Namru:2) ШО. Н.
Johnson coll.; May, 1945. One speci-
men (USNM 574210).
Mariana Islands: Guam: small pools
at zero tide, near Oca Point, D. G.
Frey coll., November 20, 1954, One
specimen (USNM 574353).
Palau Islands: inner margin of reef,
SW of Ngarduis, SE coast of Babel-
278 E. MARCUS
thuap. Sta. No. 262. F. M. Bayer coll.,
November 4, 1955. Two specimens
(USNM 575714).
Caroline Islands: Ifaluk Atoll: Helio-
pora zone south of Elangelap Id. Sta.
No. 713. F. M. Bayer coll., October
23, 1953. One specimen (USNM 574977).
Caroline Islands: [Ifaluk Atoll: in
20 feet in main pass. Sta. No. 742.
Yaniseiman coll., October 25, 1953. One
specimen (USNM 574982).
Caroline Islands: Ifaluk Atoll:
Elangelap Island. Sta. No. 626. R.
R. Rofen coll., 1953. One specimen
(USNM 574976).
Marshall Islands: Bikini Atoll: tidal
pools at tip of sand spit, western end
of atoll. Sta. No. S-42-564. 1e ei
Schultz and V. E. Brock coll., August
18, 1947. One specimen (USNM
574443).
Gilbert Islands: Onotoa Atoll: In
outer lagoon, slightly less than 4 miles
north of and 85° west of Aiaki, Ma-
neba. Sta. No. GOC 28. P. E. Cloud,
Jr. coll., July 30, 1951. One speci-
men (USNM 574933).
Gilbert Islands: Onotoa Atoll: SE
end of reef area known as Rakai Ati,
south side of big windward point of reef,
near center of atoll. Sta. No. GOC
36. PR. Cloud “Jr. coll.” August
20, 1951. One specimen (USNM 575372).
43. Phyllidia (Phyllidiella) pustulosa
Cuvier, 1804
Palau Islands: north side of Uruk-
thapel Island: in 0-7 ft. in shallow pass
between Butottoribo Id. and next island
to south, Sta. No. 27. Е. М. Bayer et al.
coll., July 20, 1955. One specimen
(USNM 575651).
Palau Islands: Iwayama Bay: in 2-3
feet on reef flat, south shore of Island
II, between shore and deep reef pool.
Sta. No. 133. F. M. Bayer et al. coll.,
August 28, 1955. One specimen (USNM
575653).
Caroline Islands: Kapingamarangi
Atoll: lagoon reef at Ringutoro Island.
Sta. No. 689. С. Handcoll., August
11, 1954.
575656).
Caroline Islands: Kapingamarangi
Atoll: Polim reef flat near Tipongowa-
karam Pass, Greenwich (Ship) Pass.
Sta. No. 724. C. Hand coll., August
12, 1954. One specimen (USNM
575654).
Caroline Islands: Kapingamarangi
Atoll: lagoon reef, Tapatuaitu Island.
Sta. No. 862. С. Hand coll., August
21, 1954. One specimen (USNM 575-
655).
Caroline Islands: Kapingamarangi
Atoll: under boulder, lagoon side of
emergent area, Tapatuaitu Island. Sta.
No. 297. C. Hand coll., July 21, 1954.
One specimen (USNM 575657): dark
green in color with white pimples.
Caroline Islands: Kapingamarangi
Atoll: lagoon reef, Tapatuaitu Id. Sta. No.
862. C. Hand coll., August 21, 1954.
One specimen in the collections of the
U. 5. National Museum.
Two specimens (USNM
44. Phyllidia (Phyllidiella) nobilis
(Bergh, 1869)
Caroline Islands: Ifaluk Atoll: under
rocks, reef flat half way between Elange-
lap and NW end of Falarik Island. Sta.
No. 378. Е. М. Bayer coll., September
21, 1953. One specimen (USNM 574-
962).
Caroline Islands: Ifaluk Atoll: from
clump of Stylophora, in 2 1/2 feet of
water at low tide, reef flat south of
Elangelap Island. Sta. No. 382. F. M.
Bayer coll., September 23, 1953. One
specimen (USNM 574963).
Caroline Islands: Ifaluk Atoll: be-
neath rocks, Heliopora zone, between
Elangelap and Ella Islands. Sta. No.
386. F. M. Bayer coll., September
23, 1953. Two specimens (USNM 574-
964).
Caroline Islands: Ifaluk Atoll: in
Heliopora zone, south of Elangelap Id.
Sta. No. 713. F. M. Bayer coll., October
23, 1953. Two specimens (USNM 574-
978).
Caroline Islands:
Ifaluk Atoll: inl
PR oe re
AL =
MICRONESIAN OPISTHOBRANCHIA
fathom on reef flat, 800 feet from shore,
west of northern end of Falarik Id.
Sta. No. 802 (R. R. Rofen Sta. 146).
Bakal, Tachim, Yarof, ©. Yark'call,,
October 29, 1953. Two specimens (USNM
574984).
Marshall Islands: Rongelap Atoll:
intertidal at Naen Id. M. W. Johnson
coll., July 17, 1946. One specimen
(USNM 574230).
45. Fryeria rüppelli Bergh, 1869
Caroline Islands: Ifaluk Atoll: be-
neath rocks, in Heliopova zone, reef
between Elangelap and Ella Islands. Sta.
No. 386. Е. М. Bayer coll., September
23, 1953. One specimen (USNM 574-
964).
Caroline Islands: Kapingamarangi
Atoll: north pass, Saratokmalei Reef,
near Teawaitua Ship Pass. Sta. No.
784. C. Hand coll., August 14, 1954.
One specimen (USNM 575692).
Suborder Dendronotoidea
Family Bornellidae
46. Bornella digitata (Adams and Reeve,
1848)
Caroline Islands: Kapingamarangi
Atoll: “microatoll”, Touhou Id. Sta.
No. 88. C. Hand coll., July 2, 1954.
One specimen (USNM 575691).
Caroline Islands: Kapingamarangi
Atoll: Sta. No.(173.)) CC. Hand. coll.,
One specimen (USNM 575695).
Family Dotoidae
47. Doto cf. albida Baba, 1955
Palau Islands: Urukthapel Island: in
2-4 feet, outer reef at eastern end.
Sta. No. 28. РЕ. M. Bayer et al. coll.,
July 21, 1955. One specimen and 1
radula slide (USNM 575673).
Suborder Eolidoidea
Infraorder Acleioprocta
Family Cuthonidae
279
48. Catriona lonca spec. nov. (Figs.
23-26)
Material: Palau Islands: Ngemelis
Islands: 1 1/2 to 6 ft. on seaward
reef flat at south end of Ngemelis Id.
Sta. No. 61. F. M. Bayer et al. coll.,
August 6, 1955. One specimen.
Description: Colorless: 1.5 mm
long. Rhinophores andtentacles smooth,
former twice as long as latter. Right
rhinophore small, in regeneration; left
tentacle wanting. Foot rounded in front,
corners not elongated; tail pointed. Ce-
rata fusiform, cnidosacs (ne) distinct.
One anterior branch of digestive gland
with 2 cerata; interhepatic space con-
taining common genital aperture (g) and
anus (ar); posterior liver with 4groups of
cerata, the two first with 2 cerata each,
the two hinder each with one ceras.
Masticatory process of mandible with
Single series of numerous high denti-
cles. Radula consists of about 40 rows.
Tooth low, median cusp receded from
cutting edge due to its insertion lying
farther back than bases of lateral den-
ticles. Number of these 5-8; size
varied. Alternate position of bigger and
smaller denticles in succeeding teeth
produces slanting rows along radula as
in Doto (Marcus, 1959, f. 158; 1960a:
168), Miesea evelinae (Marcus, 1957:
466), and Catriona maua (id., 1960a:.
179). Penis bulbar, with cuticular, 40 u
long stylet.
Holotype: slug and slide with radula,
jaw, and penial stylet (USNM 575707).
49. Catriona urquisa, spec. nov. (Figs.
27-30)
Material: Caroline Islands: Ifaluk
Atoll: washed from algae or sponge,
from 1-3 feet, patch reefon lagoon shelf,
about 75 feet from shore, Katelu area,
SW Falarik Id. Sta. No. 144-E-7. D. P.
Abbott coll., October 21, 1953. One
Specimen.
Description: Colorless: length 2 mm.
Tentacles and rhinophores smooth and of
equal size. Foot rounded in front,
280 E. MARCUS
without lengthened corners; tail pointed.
Cerata short, blunt, cnidosacs (ne) one
third of their length. Anterior liver one
horseshoe with 5 cerata, posterior diges-
tive gland with 3 rows of 3, 3 and 2 ce-
rata. Anal papilla (ar) in interhepatic
space, near first group of posterior liver.
Genital aperture (g) between limbs of an-
terior horseshoe.
Masticatory process of jaw with about
60 saw-like denticles. Radula of 21
teeth. Smallest, oldest tooth 22 u
high and broad, newest one 50 y high and
broad. First with receded median cusp
and 3 lateral denticles on each side.
In later developed teeth recession of
middle cusp less pronounced; 4-5 lateral
denticles, lower and thicker than older
ones. Minute cuticular stylet of penis
and absence of accessory penial gland
observed in sections.
Holotype: hind end of slug and two
slides: one with radula and jaw, one
with transverse sections of anterior
part (USNM 575710).
Discussion of Catriona lonca and C.
urquisa: My reason for the use of the
generic names Catriona and Cratena was
recently published (Marcus, 1960c: 258).
Only few species of Catriona have
less than 3 rows of cerata on the right
digestive gland. C. bylgia (Bergh, 1870:
4) differs by broadened jaws from the
present species; C. cucullata (Bergh,
1905: 230) by black color marks, still
present in preserved slugs. С. susa
Marcus (1960b: 916) whose tooth is
similar in shape to that of urquisa has
36 teeth with the same body length and
32 denticles on the masticatory process.
Further Indo-West Pacific cuthonids
which must be compared are En-
noia briareus Bergh (1896: 393) and
Myja longicornis Bergh (1896: 391).
The first has 2 anterior liver
FIGS. 32-36. Noumeaella rehderi, sp. n.
and denticles of masticatory process.
smooth masticatory border,
the second, one
group as lonca, but
groups,
and unarmed penis;
right liver
no stylet.
Two West Atlantic species of Catriona
with 1-2 ducts of the anterior digestive
gland (Marcus, 1957: 459; 1958: 45)
differ from lonca and urquisa by man-
dibles and radulae.
The Indo-West Pacific eolidaceans
whose position of the anus and rami-
fication of the anterior liver have not
been described were compared with
Catriona lonca and C. urquisa according
to the pharyngeal armature.
Infraorder Cleioprocta
Family Favorinidae
Subfamily Favorininae
50. Pteraeolidia semperi (Bergh, 1870)
Palau Islands: Iwayama Bay: craw-
ling on rocks among hydroids, coral
shelf, west shore of SE peninsula of Ko-
ror Id., mouth of Kakisuidó (Oyster Pass)
between Islands XXIX and east end of
Koror. Sta. No. 236 A. Е. М. Bayer,
R. R. Rofen, Rikrik coll., October 18,
1955. Three specimens and 1 slide with
radula and jaws (USNM 575658). These
animals were of a pale violet color.
Palau Islands: in 2 1/2-3 1/2 ft., at
night on reef flats south of Ngaremediu
(Raeldil) Sta. No. 254. F. M. Bayer
et al. coll., October 27, 1955. One
specimen (USNM 575659).
Caroline Islands: Kapingamarangi
Atoll: lagoon edge of lagoon reef,
Tiatua Island. Sta. No. 173. C. Hand
coll., July 13, 1954.
(USNM 575660).
Two specimens
51. Phyllodesmium hyalinum Ehrenberg,
1831
FIG. 32. Rhinophores from behind. FIG. 33. Jaw
FIG. 34. Radular tooth. FIG. 35. Diagram of repro-
ductive organs, reconstructed from serial sections. FIG. 36. Right side view.
FIGS. 37-41. Muessa evelinae, g.n., Sp.n.
FIG. 39. Radular tooth. FIG. 40. Penial stylet.
masticatory denticles.
FIG. 37. Right side view. FIG. 38. Jaw and
FIG. 41. Diagram of
reproductive organs, reconstructed from serial sections.
MICRONESIAN OPISTHOBRANCHIA 281
282 E. MARCUS
Palau Islands: in 0-1 feet, reef flat
on outer barrier reef about 2 miles
SSW of Ngaremediu District, east of
Urukthapel Id. Sta. No. 111. F. M.
Bayer et al. coll., August 19, 1955.
One specimen and slide with radula and
jaws. (USNM 575650).
52. Noumeaella rehderi spec. nov. (Figs.
31-36)
Material: Palau Islands: Ngemelis
Islands: in 1 1/2-6 ft., seaward reef
flat at south end of Ngemelis Island.
Sta. No. 61. F. M. Bayer et al. coll.,
August 6, 1955. One specimen.
Description: Colorless; length3.5 mm,
cerata 1 mm, cnidosacs 0.15 mm. Head
broad, widened laterally; tentacles short;
rhinophores with thick cluster of papil-
lae on hind side, smooth in front. Foot
projecting along body sides, anterior
border grooved, groove accompanies
projecting corners. Body tapering back-
wards. Cerata slender, in widely spaced
groups. Anterior liver a horseshoe whose
cerata are inserted in one series, inter-
hepatic space broad, containing genital
aperture (g). Posterior liver with 4
groups of cerata, the first a horseshoe,
the 3 following ones slanting rows.
Number of cerata on right (left) side:
10 (6); 9 (6), 4 (4), 2 (2), 2 (1). Anus
behind anterior limb of first group of
posterior liver.
Masticatory border of jaw with single
series of about 40 rough denticles. Ra-
dula with 18 rows, central cusp pointed,
6-7 rather short, sharp lateral denticles
on each side.
Hermaphrodite duct (h) enters short,
bag-shaped ampulla (a). Spermoviduct
(so) bifurcates some distance from outlet
of ampulla. Male duct first simple
(se) continues prostatic (q) for most of
its length; muscles of ejaculatory duct
(d) thickened to bulbar penis (p) ending
with smooth stylet. Inner oviduct (oi)
enters voluminous lobed spermatheca
(s) where sperms lie withheads attached
to wall. Vagina (v) narrow. Outlet of
gland mass (f) or nidamental duct (ni)
passes into common atrium (am) with
enormous sphincter (sr).
Named for Dr. Harald A. Rehder.
Holotype: fore and hind end of slug
in vial, and two slides: one with radula
and jaw, one with transverse serial
sections of region of gonopore (USNM
575706).
Discussion: Similar rhinopores as in
the present species occur in Berghia
Trinchese, 1877, and Baeolidia Bergh,
1888, both with pectinate radular teeth.
Among the Eolidacea with cuspidate teeth
these rhinopores are known in Moridilla
Bergh, 1888, and Noumeaella Risbec,
1937. As Moridilla belongs to the
Facelinidae and has an unarmed penis,
it cannot receive the present species.
Noumeaella curiosa Risbec (1937: 163;
1953: 159) has the same type of rhino-
phores, an armed penis, a very similar-
shaped jaw with one row of denticles,
first and second groups of cerata as
horseshoes, identical position of the
gonopore, and similar number (16) of
radular teeth with 8 denticles on each
side. Hence I infer that Noumeaella
curiosa belongs to the Cleioprocta,
though this is not evidenced in Risbec’s
system (1953: 120).
N. curiosa differs from N. rehderi
by still shorter lateral denticles of the
radular tooth and spine-like irregular
tubercles of the penial stylet.
Muessa, gen. nov.
Cleioproct Eolidacea with cuspidate
radular tooth (against Aeolidiidae), a
single branch of the right digestive gland
(liver) and its left counterpart (Favor-
inidae) and a single row of cerata on
it (Favorininae). Cerata ovoid, all in
short rows. Jaws oblong, masticatory
border with one series of few broad
denticles with rough edge. Large middle
cusp of radular tooth accompanied by
strong denticles. Penis with cuticular
stylet.
Type-species: Muessa evelinae, spec.
nov.
The annulate tentacles and rhinophores
of the type-species are not included in
the diagnosis of the genus, because the
MICRONESIAN OPISTHOBRANCHIA 283
shape, at least ofthe rhinophores, cannot
be utilized for generic distinctions in
Facelinidae and Favorinidae (Marcus,
1957: 474; 1958: 60; 1960b: 924). Never-
theless, annulate tentacles are excep-
tional even in preserved specimens of
these families.
I considered allocating the new species
to Herviella Baba (1949: 107, 180), a
favorinine genus with seriate cerata.
However, the jaw and the Globiferina-
like cerata of the present species differ
widely from the type-species of Her-
viella, H. yatsui Baba, 1949 (l. c.)
whose penial armature was not des-
cribed.
In Globiferina noumeae Risbec (1937:
163; 1953: 157) the penis is unarmed,
and the anus lies in the interhepatic
space, hence the species is acleioproct.
A singularly dentate jaw occurs also
in Phyllodesmium, but its denticles are
unlike those of the present species.
Phyllodesmium Ehrenberg, 1831, must
be added tothe Favorininae whose genera
were mentioned recently (Marcus, 1960b:
922). Its type-species, P. hyalinum,
is represented in the present collection
by a specimen from the Palau Islands.
33: Е 7: 1937: pl. 2, 8515)
gave good figures of this Species.
Ennoia longicirrha Bergh (1905: 234)
is cleioproct and may be a Cratena,
though the absence of penial armature
was not stated; evidently it belongs to
the Favorininae. Its anterior liver and
the 2 first branches of the posterior
digestive gland are horseshoes. The
acleioproct type-species of Ennoia is
mentioned here in the discussion of
the 2 species of Catriona.
53. Muessa evelinae spec. nov. (Figs.
37-41)
Material: Caroline Islands: Ifaluk
Atoll: washed from algae, intertidal
“fossil reef”, at junction of outer and
inner reef flats, east of south end of
Falarik Id., Sta. No. 83-0-4. D. P.
Abbott coll., September 29, 1953. One
specimen.
Description: Yellowish, as if it was
preserved in picric liquid; minute black
rings, principally subepidermal, onhead,
cephalic appendages, back, and some on
sides of body. Length, when extended,
3 mm, breadth 0.8 mm, cerata 0.6 mm.
Tentacles and rhinophores annulate, for-
mer longer than latter. Foot rounded
in front; tail long, pointed. Cerata egg-
shaped, cnidosacs (ne) broad. Anterior
liver one group of 3 cerata, posterior
liver with 3 groups of 3, 2 and 1 ceras.
Genital aperture (g) behind anterior
group, anus (ar) below cerata of second.
Buccal cavity with sculptured cuti-
cle. Mandible as described in diag-
nosis of genus. Radula with 14 dark
brown teeth; middle cusp broad, prom-
inent, 2-5, generally 3-4, strong den-
ticles on each side.
Hermaphrodite duct (h) dilated into
oblong ampulla (a) containing sperm.
Male (se) and female (oi) duct separate
at outlet of ampulla. Efferent duct
muscular in central, prostatic (q) in
peripheral course;, penis (p) ends with
70 uy long cuticular stylet. Male atrium
(ma) glandular, entering common atrium
(am) together with wide female duct
(eu). Vagina and nidamental duct united.
Dilatation. of female duct between gland
mass (f) and constriction of female
duct may be spermatheca, but no sperms
found in it.
Named for Mrs. Eveline du Bois-
Reymond Marcus.
Holotype: hind end of slug and two
slides: one with radula and jaws,
one with transverse serial sections
of anterior part, (USNM 575711).
LITERATURE CITED
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ELIOT; C::N2, 71903:
E. MARCUS
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der Stboga-Expedition. т Weber, M.
(ed.), Siboga-Expedition, Monogr. 50,
248 p, 20 pls.
Nudibranchiata
with some remarks on the families
and genera and description of a new
genus Doridomorpha. In Gardiner,
J. St., The fauna and geography of the
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2: 540-573, pl. 32. Cambridge.
, 1904, On some nudibranchs
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ZUSAMMENFASSUNG
UBER EINIGE MIRKONESISCHE OPISTHOBRANCHIER
Eine Sammlung des U. S. National Museums von 130 Opisthobranchiern aus Mikro-
nesien enthielt 53 Arten. Nur 10 Arten sind neu und 5 von diesen unter 5 mm lang.
Diese niedrigen Zahlen zeigen die Einheitlichkeit der indo-westpazifischen Riff-
Fauna, deren grössere Hinterkiemenschnecken grossenteils schon bekannt sind. Die
hier beschriebenen neuen Arten sind: Stiliger (Ercolania) illus, Elysia bayeri,
Elysia тата, Hypselodoris cuis, Discodoris lora, Discodoris ylva, Catriona lonca,
Catriona urquisa, Noumeaella rehderi, und Muessa evelinae, der Gattungstyp einer
neuen Gattung der Favorinidae, verwandt mit Herviella.
RESUMEN
SOBRE ALGUNOS OPISTOBRANQUIOS DE MICRONESIA
De una coleccion de 130 especimenes de opistobranquios de Micronesia pertene-
ciente al Museo Nacional de Estados Unidos, y compuesta de 53 especies, sólo 10
eran neuvas y la mitad de estas de longitudes menores a 5 mm. Esta pequeña
cantidad señala la uniformidad de los opistobranquios en los arrecifes del Océano
286
E. MARCUS
Indo-Pacifico occidental, cuyas especies de mayor tamafio son en su mayoria cono-
cidas. Se describen las siguientes especies: Stiliger (Ercolania) illus, Elysia bayeri,
Elysia ratna, Hypselodoris cuis, Discodoris lora, Discodoris ylva, Catriona urquisa,
Noumeaella rehderi, y Muessa evelinae especie tipo de un género nuevo de Favorin-
idae, afin to Herviella.
RESUMO
SOBRE ALGUNS OPISTHOBRANQUIOS DA MICRONESIA
Entre 130 lotes de opistobranquios da Micronésia, pertencentes ao U.S.
National Museum, houve 53 especies das quais apenas 10 s4o novas. O comprimento
da metade das últimas é aquém de 5 mm. Estes números baixos mostram a uni-
formidade da fauna dos opistobránquios dos recifes no Indo-pacífico ocidental,cujas
especies maiores ja se conhecem, em grande parte. As novas espécies aqui des-
critas s4o: Stiliger (Erocolania) illus, Elysia bayeri, Elysia тата, Hypselodoris cuis,
Discodoris lora, Discodoris ylva, Catriona lonca, Catriona urquisa, Noumeaella
rehderi, e Muessa evelinae, o tipo dum novo género das Favorinidae, parente de
Herviella.
MALACOLOGIA, 1965, 3(2): 287-307
“GROWTH RINGS” IN THE BEAKS OF THE SQUID 1
MOROTEUTHIS INGENS (OEGOPSIDA: ONYCHOTEUTHIDAE)
Malcolm R. Clarke
National Institute of Oceanography,
Wormley, Godalming, Surrey, England
ABSTRACT
The present work, which describes cycles of growth lines (microrings) in the
lower beaks of Moroteuthis ingens, intends to draw attention to the possibilities
of relating cycle formation and time of growth of the squid. The study is based
опа large sample of beaks collected from stomachs of sperm whales caught at
Durban. Features used in identification (Fig. 1) are described. On the medial
surfaces of the lateral walls of these beaks 4 features are visible (Fig. 2):
ridges radiate from the rostral tip to the free edge and, running parallel with
the free edge, there are minute steps or microrings, undulations and “lines” of
varying transparency. Microrings constitute a record of the extension of the la-
teral wall during growth. Cycles of microring width between the rostral tip and
the free edge can be recognised. Variation in the form of cycles in 50 beaks is
described and it is shown that the first 3-4 cycles usually follow a definite pat-
tern while later cycles vary considerably (Fig. 3). Very little wear of the ros-
tral tip takes place during life in the size range studied (rostral length 0. 7-2.0
cm). Frequency histograms and means of the number of microrings in each
cycle show that cycles cannot be formed by random fluctuations of secretion
5 alone even if such fluctuations were biased by later cycles being narrower than
earlier cycles. Beak growth can be conveniently expressed as increase in wall
length, which is the distance from the rostral tip to the anterior and inner cor-
ner of the lateral wall (Fig. 2). Since the history of the growth in wall length is
recorded by the distance of the microrings from the rostral tip, growth may be
“back-calculated”. Increase in beak size with increase in the number of cycles
has been plotted, as well as a back-calculated curve not subject to any bias due
to selection by the whale (Fig. 8). Back-calculated wall lengths from older beaks
(more cycles) give lower values than those from younger beaks probably because
the more slowly growing squids survive longer. The relationship between wall
length and the size of the squids has been plotted (Fig. 10, 11). Thetimetakenfor
a cycle to be secreted has not been established, but tentative reasoning, based
en previous studies of other cephalopods, suggests 6 or 12 months.
INTRODUCTION groups or the analysis is complicated
by migrations. However, growth has
Little information is available on the been studied in several cephalopods
growth of cephalopods: they dc not which are found on the continental shelf
live for long in aquaria and field sam- at some time during the year, notably
ples are either too small to show age in the loliginids Loligo vulgaris, by
1
This paper is based on part of a talk given at the “Symposium on the Mollusca” of the Zoologi-
cal Society of London, on the 5th of March, 1964.
(287)
288 M. R. CLARKE
A INNER
wing
medial surface of wing
fold of hood-wing
structure
rostral edge
rostral tip
rostrum hood
OUTER
medial surface of right
lateral wall
inner edge of left lateral wall
free edges
posterior edge of left lateral wall
POSTERIOR
lateral surface of left lateral wall
fold of lateral wall
FIG. 1. A diagram of the lower beak of Moroteuthis ingens to show the terms used in the text.
Terms underlined describe features characteristic of onychoteuthid beaks. Large arrows indi-
cate surfaces upon which material is deposited during growth. Small open arrows indicate the
growing edges.
Tinbergen and Verwey (1945), and Lo-
ligo opalescens by Fields (1950, 1963);
the ommastrephids Шех illecebrosus by
Squires (1957), Ommastrephes sloanei
by Katoh (1959), and Todarodes sagit-
tatus by Fredriksson (1943); and the
octopod Eledone cirrosa by Wirz (1963).
Growth in these species has been studied
by examining the size groups in the pop-
ulation and by finding the shift in the
mean size through the year. Both
these methods have disadvantages which
would be avoided if some method of
age determination, similar to scale or
otolith reading in fish, could be dis-
covered. Such a method has been found
in some species of Sepiidae, as pointed
out by Yagi (1960) and Choe (1963),
who have shown the average number of
days in which a growth “stripe line”
in the cuttle bone is secreted. In order
to find a method of age determination
Tinbergen and Verwey (1945) examined
the beaks of Loligo vulgaris and Wirz
(1963) examined beaks and radulas of
various cephalopods: no method was
discovered.
The present work describes cycles of
growth indicated by “growth lines” or
microrings on the lower beak of Moro-
teuthis ingens. It has not proved pos-
sible so far to identify these with time
of growth. Similar cycles are present
in beaks of many species and this des-
cription is intended to draw attention
to them so that a correlation between
time and cycle formation can be investi-
gated in species at present being studied
by other workers.
DESCRIPTION AND MATERIAL
The descriptive terms used in this
paper are evident from Figs. 1 and 2.
GROWTH RINGS IN BEAKS OF MOROTEUTHIS 289
Most of these have already been defined
(Clarke, 1962) but it has been necessary
to introduce several new terms for the
present purposes. Surfaces facing the
sagittal plane of the beak and animal
are termed medial, those facing away
from the sagittal plane are lateral; the
inner side is that which lies towards
the upper beak when in situ andthe outer
side is that which lies away from it.
The lower beak is bilaterally symme-
trical with each half consisting of several
thin chitinous sheets: a lateral wall is
fused along its anterior border to a hood
with an inward extension beyond the la-
teral wall termed the wing. A small
trapezoid or triangular sheet of chitin
joins the lateral wallatits inner anterior
corner to the wing and this has been
called the medial surface of the wing.
The jaw angle is the angle between the
medial surface of the wing and the ros-
tral edge formed by the fusion of the
lateral wall and the hood. The rostrum
is a term derived by analogy with the
upper beak in which its limits are dis-
tinct and here it is used generally to
mean the part of the beak from the jaw
angle to the rostral tip including the
hood and the anterior part of the lateral
wall. The wall length is the distance
from the rostral tip to the inner anterior
corner of the lateral wall (Fig. 2).
The present study is based on beaks,
identified by the author as those of
Moroteuthis ingens, taken from the sto-
machs of 14 sperm whales caught off
Durban, South Africa in 1962 and 1963.
Of these, sub-samples of the beaks
collected from a whale killed in June
1962 and another killed in September
1962 were selected for a more detailed
examination. All the beaks were not
Suitable for all parts of the study and
fewer beaks were necessary for certain
purposes. A maximum of 292 anda
minimum of 39 beaks were used for
various parts of the detailed morpholo-
gical work.
The beaks of 2 other onychoteuthid
Species, Moroteuthis robsoni and
Tetronychoteuthis sp., were also present
in the stomachs. While the beaks of
these latter species were associated with
flesh, those of M. ingens were entirely
devoid of flesh and this may suggest that
they had been ingested some time pre-
viously in the Antarctic, where the spe-
cies is found intact in whale stomachs.
For identification, lower beaks from
the Durban whales were compared with
beaks from complete specimens ofthese
3 species as well as with beaks of 2
other onychoteuthid species.
Features distinguishing the beaks of
the family Onychoteuthidae (underlined
in Fig. 1) are briefly: a clearly de-
fined fold of the lateral wall; an obtuse
jaw angle; a jaw angle which is hidden
from the side by the forward protrusion
of the hood-wing structure; a slight step
between the medial surface of the wing
and the anterior end of the lateral wall
due to the fact that the inner end of the
rostral edge lies inside and medial to
the point where the shoulder is inserted
into the rostrum; and the hood is short
from front to back compared with the
crest.
Moroteuthis beaks are further charac-
terised by having a fold of the lateral
wall which intersects the posterior edge
at about half way between the crest and
the inner edge of the wall (also noted
in Clarke 1962).
Moroteuthis ingens and M.robsoniare
the only species of this genus known to
occur in Antarctic or South African
waters and this supports the identifi-
cations.
If the lower beak of Moroteuthis in-
gens is cut on the left side ofthe rostral
tip and the medial surface of the lateral
wall so exposed is viewed by oblique
reflected light, 3 features can be seen
(Fig. 2, A). Ridges radiate from the ros-
tral tip to the inner and posterior, free
edges of the wall, while 2 other features
which may be described as undulations
and microrings run roughly parallel with
these free edges. The latter 2 features
are diagrammatically represented in
Fig. 2, B. In addition, “lines” of varying
colour or transparency, which corres-
290 M. R. CLARKE
Icm
eee
radiating
ridges
undulations
microrings
one microring
ES, variation in
transparency
QA A
undulation
FIG. 2. A. The medial surface of the right lateral wall exposed to show the microrings, undula-
tions and radiating ridges. The limits of 7 cycles are indicated by numbers in white areas.
Cycle 3 contains the stable region. Limits of the wall length and rostral length are shown.
B. A short section of the lateral wall cut along a radiating ridge adjacent to the free edge. It is
not to scale and merely illustrates the terms “microring”, “undulation” and “variations in trans-
parency”.
GROWTH RINGS IN BEAKS OF MOROTEUTHIS 291
pond in position to the microrings,
are visible by transmitted light near
the free edge of the lateral wallin this
species.
The microrings constitute a record of
the extension of the lateral wall during
the growth of the beak.
The beak is secreted by an epithelium
which adds chitinous material on the pos-
terior side of the hood and wings and on
the lateral side of the lateral wall (sur-
faces indicated by large arrows in Fig.
1). As growth proceeds, the secreting
area expands so that the chitinous ma-
terial overlaps the edges of the growing
surface (edges indicated by small open
arrows in Fig. 1). This overlapping
gives rise to the microrings on the me-
dial surface of the lateral wall, which
are really minute steps suggesting that
growth is not a steady, continuous pro-
cess. In surface view the flat part of
each step (microring) is limited by 2
thin “lines”, the vertical components of
adjacent steps. The width of the micro-
rings varies and the variations occur
in a series of cycles running from the
rostral tip to the free edges of the la-
teral wall (Fig. 2). This cyclic arrange-
ment is indistinct in some regions
of nearly every beak, but by careful
examination, it has proved possible to
find cycles along the lengths of over
99% of the beaks examined. The ar-
bitrary limit of each cycle has been
taken as the posterior margin of the
broadest microring in that cycle (Fig.
3). The mean width of the cycles gradu-
ally decreases from the rostral tip to
the free edges of the lateral wall. Be-
Sides this decline, which is not usually
regular, there are several possible
variations in the microring composition
of the cycles (Fig. 3). Table 1 sum-
marizes the results of examining the
cycles of 50 beaks and provides infor-
mation for a rough general outline of
the “usual” course of growth inthe beak.
It must be stressed that all possible
intermediates exist between these forms
¡and their grouping is, therefore, rather
| subjective.
N y
ЕЕ IA
Е ee
; y
АДД ААА АПУ
у =
PET TT TIM TT TTT
(i to ge oe
e y
LITE DDN
EEC нев
FIG. 3. Diagrams to illustrate different types
of cycle. The upper figures represent a sur-
face view and the lower figures indicate the
increasing or decreasing fluctuations in width
of the microrings. Cycle limits are indicated
with arrows. A. Two cycles showing agra-
dual increase and then a sharp decrease at the
onset of the next cycle. B. Two cycles show-
ing a steady decrease and then a steady in-
crease. C. Twocycles showing a steady de-
crease followed by a sharp increase at the on-
set of the next cycle. D. Two cycles showing
little change except for a marked increase at
the last microring.
Often, the 2 earliest cycles (i. e.,
nearest the rostral tip) do not have
step-like microrings but only undula-
tions. However, these undulations may
be considered as microrings for our
purposes because, in some beaks, both
undulations and microrings are present
and they coincide very closely in ar-
rangement and position. From the first
(earliest) one visible, the microrings
gradually increase in width to the end
of the first cycle. This type of cycle
292 M. R. CLARKE
30
25
20
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a
at 15
O
o
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10
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N° OF MICRORINGS FROM LAST BROADEST
TO EDGE
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LOWER ROSTRAL LENGTH N® OF MICRORINGS IN STABLE
REGION
FIG. 4. A. Frequency histograms to show the number of microrings between the limit of the
last full cycle and the free edge of the lateral wall. A sample of 53 beaks taken in September
(hatched) and a sample of 175 beaks taken in June are shown; mean values are indicated by ar-
rows. B. A plot of the number of microrings between the rostral tip and the first microring of
the “stable” region against the rostral length in a sample of 39 beaks. The mean number of mi-
crorings to the start of the “stable” region is indicated by an arrow. C. Frequency histogram
showing the number of microrings in the “stable” region. The mean value is indicated by an
arrow.
GROWTH RINGS IN BEAKS OF MOROTEUTHIS 293
and a rough indication of changes in
growth of the microrings is shown in
Fig. 3, A. The second cycle is in
general, similar in form to the first.
In the second or third cycle a num-
ber of microrings have a very uniform
width and in 80% of (46) beaks there
are 3-12 microrings which are equal
in width (Fig. 4, C). The position of
the first microring of this “stable”
region varies from the 7th to the 34th
microring counted from the rostral tip
in the sample (39 beaks) examined (Fig.
4, B).
Following this “stable” region, there
is nearly always a cycle which varies
from beak to beak but is characterised
by having some extremely narrow, in-
conspicuous microrings. Up to this
point the undulations have more or less
coincided with the. microrings but from
here onwards undulations very roughly
approximate to the cycles in position.
This cycle, which is usually the fourth
(but is sometimes the third), is easily
recognised because it consists of a
broad undulation with very minute micro-
rings on it. It, and the following (later)
cycles can all take any of the forms
shown in Fig. 3, A-D or intermediate
forms but there is a tendency towards
type D in the later cycles of the older
beaks (Table 1).
WEAR OF THE BEAK
Clearly, if the lateral wall is worn
away at the rostral tip to any appre-
ciable extent,the cycles cannot be uti-
lised for age studies. Fortunately,
in the size range examined (lower ros-
tral length 0.7-2.0 cm), wear is not
appreciable. If microrings did dis-
appear by wear, there would be a nega-
tive correlation between the number of
microrings between the rostral tip and
the stabla region and the size of the
beak (as shown by rostral length) and
such a correlation is not found (Fig.
4, B based on 39 beaks). Nor is such
a negative correlation found when the
distance from the rostral tip to the end
TABLE 1. Types of cycles observed in 50*
lower beaks of Moroteuthis ingens
Position of
cycle from
rostral tip
Totals2
2Totals are not 50 for all cycles given in this
table because some cycles were too indistinct
to recognise which type of microring con-
figuration was present.
3Types as in Fig. 3.
of the first cycle is plotted against the
rostral length. Further evidence sug-
gesting the loss of few if any micro-
rings is that the microrings curve away
from the rostral tip just prior to meeting
the jaw edge (Fig. 2, A) and, although
the distance between the inflection and the
jaw edge does decrease towards the ros-
tral tip, only the few microrings nearest
the tip have lost the inflection altogether.
Thus, if loss of microrings does occur,
few are involved and we can be con-
fident that no complete cycles are lost
during the growth of the beak in the size
range examined here. How many early
cycles are not represented in these
beaks is not known.
MICRORINGS IN EACH CYCLE
The number of microrings in each
cycle were counted and the means,
standard deviations and standard errors
were found for each cycle counting from
the tip to the free or growing edge
(Table 2; Fig. 5). To avoid subjec-
tivity, the limits of cycles were always
marked with white ink before micro-
rings were counted. Frequency histo-
294 M. R. CLARKE
16 218 140 139 126 Ю 95 86 62 38 2! 2 6 2 |
D
о
№. ОЕ MICRORINGS
œ
o) 2 4 6 8 10 12 14
CYCLE No
FIG. 5. Number of microrings in successive
cycles. Means (circles), standard deviations
(lines) and the number of beaks are indicated.
grams (Fig. 6) of these same counts
show a great range with peaks at from
12 in the 1st cycle to about 8 in the 11th
cycle; their means are between 8 and 12
(Fig. 5) and they are not conspicuously
skewed in either direction. These 3
properties of the histograms (i.e. mode
at 8-12, mean at 8-12 and lack of any
definite skewness) enable us to see
whether the cyclic pattern could arise
merely by random fluctuations in se-
cretion or if we must look for some
other reason for their existence. Ifran-
dom fluctuations of secretion produced
the cycles, each microring would have an
equal opportunity of being either broader
or narrower than the previous microring
formed. One would then expect a large
number of cycles to consist of only 2
microrings because, from the definition
of a cycle, a new cycle is started when
a narrower microring follows a broader
microring. One would not expect every
cycle to consist of 2 microrings; but,
if the number of microrings in each
cycle were plotted as a histogram, one
would expect a number of cycles with 2
microrings andthena decreasing number
with 3, 4, 5 etc., microrings, i.e., a
positively skewed distribution with a
mode at 2. Further, if the mean num-
ber of “microrings” in each“cycle”is
calculated for this skewed distribution,
it is found to be about 4 “microrings”
per “cycle”. (This was checked by
tossing a coin, taking ‘obverse’ to re-
present broader than the previous micro-
ring and ‘reverse’ to represent narrower
than the previous microring. Every time
the reverse followed the obverse a
“cycle” was commenced and the number
of tosses in each “cycle” gave the num-
ber of “microrings”). Thus, the dis-
tributions derived by counting the num-
ber of microrings in each cycle of the
beaks have a different mode, mean
and skewness to any cyclic pattern which
could arise from unbiased random fluc-
tuations in secretion.
The cycles which are first formedare
broader than the later cycles. This may
be seen by reference to Fig. 8 in which
the back-calculated mean wall lengths
are plotted. The latter are found by
measuring from the rostral tip to suc-
cessive cycles. It will be seen that a
line drawn through the means, curves
downwards towards the cycles formed
more recently, i.e., cycles secreted
early in life are broader than those se-
creted later. This fact. suggests that
there may be a bias during microring
formation and this could result incycles
having more microrings. If such a bias
Operated and a microring was more
likely to be narrower than the previous
microring secreted, one would expect
many cycles to consist of microrings
steadily decreasing in size until the
last one, which would be larger, i.e.,
FIG. 6. Frequency histograms showing the number of microrings in successive cycles. The left
hand black arrow indicates the mean if chance alone was operating; the right hand arrow, the
mean. The broken line shows the simulated distribution with a mean of 11-12 (see text).
a Fe „a
FREQUENCY
NO
GROWTH RINGS IN BEAKS OF MOROTEUTHIS 295
EE
И
10
20
20
20
40
30
7 = ERES |
52076. 232% AOS ISA 20 22223 24
No. OF MICRORINGS IN EACH CYCLE
296 M. R. CLARKE
TABLE 2. The number of microrings in the various cycles
No. of
beaks in
samples
(N)
Mean No.
of micro-
rings
(x)
Cycle
as in Fig. 3, C. Because such a pat-
tern is not found in the beaks (Table
1), we can be fairly confident that the
cycles do not arise in this way. How-
ever, recognition of the types of cycle
is rather subjective and additional evi-
dence is desirable. To test whether
bias can give a normal-type distribution
with a mean similar to that obtained
when frequency histograms of the num-
ber of microrings in a cycle are plotted
(Fig. 6), a simple experiment was con-
ducted.
Bricks of 2 colours were drawn from
a bag in which sufficient were present
to overcome any effect due to removal
of the sample. In the trials the bricks
were present in different ratios and the
minority colour was taken to repre-
sent the event of a microring being
broader than its predecessor and the
majority colour was taken to represent
the event of it being narrower. By
trial and error it was found that when
the bricks were in a ratio of 9.5:1 the
mean number of “microrings” per cycle
was very similar to that in cycle 1
of the beak, i.e., between 11 and 12.
The shape of the distribution, however,
was very positively skewed (Fig. 6)
and this shows that bias alone cannot
be the main factor in producing cycles
in the beaks.
Standard
Varlahee Standard error of
9 deviation mean
(s ) (s) (sz)
en Bo D IN Go go po go go co go go
oO NN I © © =] © J © ©
CYCLES AND WALL LENGTH
Wall length has the advantage over
other dimensions of the beak, that the
history of its growth is recorded by the
position of the microrings near the ros-
tral edge. Thus, by measuring the dis-
tance from the rostral tip to succeeding
cycle limits, the increase in wall length
during particular cycles can be found.
Frequency distributions of wall
lengths, separated according to the total
number of cycles in the beaks, show
the increase in size with increase in
the number of cycles (Fig. 7). The
means of these distributions are plotted
as crosses in Fig. 8 (Table 3). These
means are affected by non-randomness
of the sampling. If the whale selectsthe
larger young squids, one would expect
the curve to be flattened because the
means of wall lengths of the younger
beaks with fewer cycles would be higher
than the means of the population. That
such a bias is involved is suggested by
comparing the crosses with the back-
calculated growth curve (circles, lower
curve Fig. 8, Table 4) which is not
subject to such a bias. The back-
calculated curve is found by measuring
from the rostral tip to the limits of
every cycle in every beak (150 beaks)
and then calculating the mean position
GROWTH RINGS IN BEAKS OF MOROTEUTHIS 297
ye 23
CYCLE
ae
del 40
Où
he 45
9.150
ve 50
8
20
5
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9 O
37
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40 26
? 201
40 23
+ 201-
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50
КОРЕЕ а 2176777:87 52:07 2:27 724772672830 3-2 3-4
WALL LENGTH (in cm)
FIG. 7. Frequency histograms showing the wall length in beaks with different numbers of cycles.
The number of beaks in each sample is given to the right of the figure.
298 M. R. CLARKE
TABLE 3. Wall length and the total number of cycles in 292 beaks
Standard
Variance Standard error of
deviation mean
(s) (sz)
TABLE 4. Back-calculated? wall lengths
Mean wall
No. of length at
beaks in each cycle
sample in cm
(N) ® (s°)
Variance Standard
deviation
(s)
Cycle
D D 0 ND M M M RP RB
A
4The back-calculated wall lengths are found by measuring from the rostral tip to every cycle li-
mit in each beak means
GROWTH RINGS IN BEAKS OF MOROTEUTHIS
WALL LENGTH
HION37 37LNVN 71VSHOQ
о.5
CYCLE Мо
FIG. 8. Growth curves of Moroteuthis ingens
derivedin different ways from the lower beaks.
Crosses show the mean values of wall length
plotted against the total number of cycles in
the beak. Open circles show the means derived
by measuring the distance from the rostral tip
to each successive cycle in 161 beaks i.e., the
circles show the back-calculated length at suc-
cessive cycles (Table 4). Standard deviations
are represented by vertical lines. Dorsal man-
tle length values (right ordinate in cm) were
found from the relationship between wall length
and dorsal mantle length given in Fig. 10.
for each cycle limit. The position of
this curve depends to some extent on
the composition of the sample because
back-calculated wall lengths from older
beaks (more cycles) give lower values
than from younger beaks (Table 5 and
Fig. 12). The same situation was found
by Lee (1912) when fish scale size was
back-calculated. It is accounted for by
the fact that the fish which grow more
Slowly survive longer and the same
explanation probably holds good for
squids.
Frequency histograms of the back-
calculated wall lengths at each cycle
are given in Fig. 9. A difference in
size of the 2 sexes could account for
299
the bimodality of the histogram for
cycle 1.
BEAK AND SQUID GROWTH
Growth of the beak is of only very
limited interest unless it can be related
to growth of the animal. Fig. 10 shows
the relationship between the wall length
and the dorsal mantle length (roughly
about half the total length) based on the
only available data for the family. The
line is drawn in to suggest the likely
course of growth of Moroteuthis ingens
which is represented by the black circles.
The 3 open circles which lie well off
the curve represent M. robsoni which
has a very pointed (i.e. long) mantle.
More specimens are required to verify
the curve suggested. A double loga-
rithmic plot of the weight of the squid
against the wall length reveals a linear
relationship (Fig. 11). By direct com-
parison, therefore, it is possible to find
the lengths or weights of squid at dif-
ferent beak sizes and a dorsal mantle
length scale has been added to the right
of Fig. 8.
TIME AND GROWTH
Clearly, the length of time taken for
the beak to grow through one cycle
could be established if the increase in
microrings between 2 samples taken a
few months apart could be found. To
this end, the microrings between the limit
of the last cycle and the free edge of
the lateral wall were counted in beaks
taken from a whale caught in June and
a whale caught in September of the same
year (1962). The counts of the 2 sam-
ples were then compared to find any
increment in the number of microrings
over the 3 months period (Fig. 4, A).
Means for these counts were 7.7 and
7.5 for the June and September samples
respectively. The samples were not
significantly different. However, from
frequency histograms (Fig. 13) there is
evidence that the size composition of
the population sampled differed in the
300 M. R. CLARKE
20 25
CYCLE
10 10
20 42
Ня го
20
See
20
го
O
S- 20
>
ui m0
FL
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Gi
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mu 20 117
5
4 134
3 149
2 149
148
|
192
Pre oe le i Nordea ia sere a UU
1 23 45 6 7 8 9 WH 1213 14 5 K I7 18 19 2021 22 23 24 25
BACK CALCULATED WALL LENGTH
(in cm)
FIG. 9. Frequency histograms (%) showing the back-calculated wall lengtns at each cycle. The
number of beaks in each sample is given to the right of the figure.
GROWTH RINGS IN BEAKS OF MOROTEUTHIS 301
TABLE 5. The mean distance in mm from the rostral tip to each successive cycle in each age
group (67 beaks)
Total number of cycles and number of beaks in sample (N)?
. e а | ee
.79 к . 59
.95 я . 68 (12)
. 14 $ . 50(10)
. 14(13)
. 28 (12)
5In those few instances where means were based on a different number of beaks,
is given in parentheses after the wall length.
2 months and this fact, coupled with
the extreme difficulty in counting the
very narrow microrings on the edge,
probably accounts for this failure to
find any increment.
cm ©
90
80
70
60
50
DORSAL MANTLE LENGTH
0 1-0 2:0 3-0 cm
WALL LENGTH
FIG. 10. Relationship between wall length of
the beak and dorsal mantle length of onycho-
teuthids determined by removing beaks from
Black circles are Moroteu-
identified squids.
this ingens. Line drawn in by eye (see text).
the value of N
DISCUSSION
If we consider other methods of study-
ing growth several disadvantages are
at once apparent. Most previous work
on cephalopods has depended on finding
the change in the mean size of the popu-
lation through the year. If the mean
size becomes larger, then there is a
temptation to interpret the shift as
growth; but it must be remembered that
this could equally well be due to mi-
gration of larger individuals into the area
or smaller individuals out of the area
towards the end of the period sampled.
Another method employed in studying
growth is Petersen’s method of finding
the peaks, which may represent age
groups in a population sampled over a
brief part of the year. This method
has also been used to study cephalo-
pods (Wirz, 1963; Fields, 1963) but, as
pointed out by Wirz, the animals so stu-
died must have a rather brief breeding
season so that successive broods are
easily distinguished by the size and all
ages must be present in the sample.
Age determination from laminations
of some kind would overcome these
difficulties.
302 M. R. CLARKE
20,000
10,000
1,000
WEIGHT IN GRAMS
100
‘| A LS 5.18910 2:0 30 40
WALL LENGTH
FIG. 11. Logarithmic plot showing the relationship between wall length of the beak and total
weight of onychoteuthids determined by removing beaks from identified squids. Line drawn in by |
eye.
303
GROWTH RINGS IN BEAKS OF MOROTEUTHIS
TABLE 6. Increment in mantle length during the first 3 years of life of cephalopods previously studied and also the deduced increment in
the mantle length of Moroteuthis ingens, estimated from the back-calculated curve of the beaks, assuming 1 cycle on the beak
to represent varying spans of time in the life of the squid
Increment in mantle length
alcala”
mantle length
in cm
Tinbergen 25. 0
Fields 16.5 3
Author 2nd year
% of max.
3rd year
cm % of max.
Species
Loligo vulgaris с’
Loligo opalescens &
Loligo opalescens & Fields 15.0 3
Illex illecebrosus с’ Squires 2
Illex illecebrosus Y Squires 2
Eledone cirrosa Wirz 255
Moroteuthis ingens (10 cycles)
If 1 cycle were formed in 1 month
If 1 cycle were formed in 4 months
If 1 cycle were formed in 6 months
If 1 cycle were formed in 12 months
i.e. the mean value of the oldest “age group” given in the papers quoted.
i.e. the age of the oldest group given in the papers quoted.
Possibly less than a year’s growth.
6
7
8
9
From squid caught in May but probably from a second year age group.
10From 2 squids caught in May but probably from a second year age group.
304 M. R. CLARKE
cm и (3)
О
2-0 ;
У: cas
e ой
7 974) /
= J
oo /
5(14)x/ -
1-5 “8 4
3(4) : и
Е I xs /
z
=
=
=
КО
<
tu
=
0-5
CYCLE N®
FIG. 12. Back-calculated mean wall lengths for
each cyclefound by examining separately beaks
with 3, 5, 7, 9 or 11 cycles on the lateral wall.
This figure shows that back-calculation from
older beaks (with more cycles) suggests a
slower growth than back-calculation from
younger beaks and illustrates part of the data
given in Table 4. The number of beaks meas-
ured is given in brackets for each curve.
The present study has not shown the
time taken for a microring or a cycle
to form, but some of the possible al-
ternatives seem unlikely on the basis of
work previously done on other species.
It seems likely that the microrings
are secreted in a discrete time inter-
val and vary in width according to some
environmental influence such as food
supply or temperature.
Table 6 summarises the increment in
mantle length of the species of squid
previously studied in detail as well as
the increment estimated from the back-
calculated curve of Moroteuthis ingens
beaks, if we assume a cycle to be se-
creted in 1, 4, 6 or 12 months res-
pectively. It will be seen from the table
that, if a cycle only takes 1 month to
form, the growth would have to be about
4 times the maximum growth known in
squids and the largest M. ingens would
be less than a year old. This seems
unlikely. If a cycle is secreted in 4
months, the annual increment in size
would be about twice as much as that
of Loligo vulgaris; the largest M. ingens
would take 3 years to grow and we
know that L. opalescens does survive
that long. It is, however, difficult to
envisage what environmental influence
could operate over 4 months although
a combination of factors could possibly
do so. It is easier to picture environ-
mental influences affecting the growth
over 6 months or a year. If a cycle
is secreted in a year the annual incre-
ment in size would be similar to that
met in L. vulgaris males, but this would
mean that M. ingens survives for at
least 10 years.
When the increment in length for each
year is expressed as.a percentage of
the mean length of the oldest age group
found (underlined, Table 6), the species
previously studied show certain simi-
larities to one another. The growth
during the first year amounts to 39-
62% and that of the second year to 32-
41% of the length reached in the final
year. In Moroteuthis ingens, if a cycle
represented 4 or 6 months, the first
year’s growth would be similar to that
of the other species (53% or 40% res-
pectively) but the 2nd year’s growth
would be much less than that ofthe other
species (21% instead of 32-41%). In
fact, whether 1 cycle represents 1, 4,
6 or 12 months’ growth, it is clear that
Moroteuthis ingens is rather dissimilar
in this respect from the other species.
Certain cycles are very similar in
different beaks. The first 2 cycles
usually have the type A (Fig. 3) form,
and this may suggest more regular
feeding or environmental fluctuations
than are found in later cycles. The
“stable” region mentioned (2nd or 3rd
cycle) may suggest stable feeding or con-
ditions for the period of its formation.
GROWTH RINGS IN BEAKS OF MOROTEUTHIS 305
10 1X
(3)
20
10 Vu
(2)
SO
so
40
Vil
30 (4)
20
n 10
ul
о ==
78 (2
WZ
3
2,100
œ
u
90
80
70
60 VI
(3)
SO
40
30
20
10
== =
20
У
10 (2)
7 -8 9 1O 1-1 12 13 14 1-5 1-6 17 +8 19 20 cm
LOWER ROSTRAL LENGTH.
FIG. 13. Frequency distributions to show the rostral length of the lower beaks of Moroteuthis
ingens taken from stomachs of sperm whales caught off Durban between May and September 1962
and 1963. The months are indicated by Roman numerals and the number of whales from which
samples were removed in each month is given in brackets.
306 M. R. CLARKE
An interesting point not mentioned so
far is that very few of the beaks have
undarkened wings and, if such darkening
is correlated with attainment of sexual
maturity as it is in the Ommastrephidae
(Clarke, 1962), the sample would consist
of mature squids almost entirely.
ACKNOWLEDGMENTS
The author is very grateful to Dr.
A. Bidder and Mr. R. I. Currie for
helpful criticism of the manuscript and
Mr. J. Bannister and Mr. R. Gamble
who went to considerable trouble in
collecting the squid beaks used in this
work.
REFERENCES
CHOE, S., 1963, Daily age markings
on the shell of cuttlefishes. Nature,
Lond., 197: 306-307.
CLARKE, M. R., 1962, The identi-
fication of cephalopod “beaks” and
the relationship between beak size
and total body weight. Bull. Brit.
Mus. (nat. Hist.) (Zool.), 8 (10): 421-
480.
FIELDS, W. G., 1950, A preliminary
report on the fishery and on the bi-
ology of the squid, Loligo opalescens.
lescens. Proc. XVI International Con-
gress of Zoology, 1: 72.
FREDRIKSSON, A., 1943, Remarks on
the age and the growth of the squid.
Greinar, 2: 2-4.
KATOH, G., 1959, A few comments on
the biological grouping of the common
squid derived from its ecological as-
pect-1. Rep. Japan Sea reg. Fish.
Res. Lab., 5: 1-17.
LEE, R. M., 1912, An investigation
into the methods of growth deter-
mination in fishes. Publ. Circ. Cons.
Explor. Mer, 63: 1-35.
SASAKI, M., 1921, On the life history
of an economic cuttlefish of Japan,
Ommastrephes sloani pacificus.
Trans. Wagner Free Inst. Sci. Philad.,
9 (2): 1-25.
SQUIRES, H. J., 1957, Squid, Illex
illecebrosus (Le Sueur) in the New-
foundland fishing area. J. Fish. Res.
Bd. Can., 14: 693-728.
TINBERGEN, L. and VERWEY, J., 1945,
Zur Biologie von Loligo vulgaris Lam.
Arch. neerl. Zool., 7 (1 et 2): 213-
286.
WIRZ, K. M., 1963, Biologie des Cé-
phalopodes benthiques et nectoniques
de la Mer Catalane. Vie et Milieu,
Suppl., (13): 1-285.
YAGI, T., 1960, On the growth of the
shell in Sepia esculenta Hoyle caught
Calif.
Fish & Game, 36: 365-377.
‚ 1963, Biology of Loligo opa- Fish., 26 (7): 646-652.
RESUMEN
ANILLOS DE CRECIMIENTO EN LAS MANDIBULAS DE MOROTEUTHIS
El presente trabajo, que describe los ciclos de lineas de crecimiento (micro-
anillos) en la mandibula inferior de Moroteuthis ingens, intenta llamar la atenciön
sobre la posibilidad de relacionar la formación cíclica con el tiempo de crecimiento
del calamar. El estudio se basa еп un gran número de muestras de los picos obtenidos
del estomago de cachalotes cazados en Durban. ‘Se describen los rasgos usados en la
clasificación (Fig. 1). Sobre la superficie media de la pared lateral.en los picos hay
4 caracteres visibles (Fig. 2): costillas que irradian desde la punta rostral al borde
libre, y diminutos microanillos, ondulaciones y “lineas” de transparencia variable que
corren paralelas a ese borde. Los microanillos constituyen un registro de la exten-
sión de las paredes laterales durante el crecimiento. Pueden reconocerce ciclos en el
ancho de los anillos entre la punta rostral y el borde libre. En 50 picos observados
la variación de los ciclos muestra que los 3-4 primeros ciclos generalmente siguen un
patrón definido mientras que los últimos varían considerablemente (Fig. 3). Durante
in Tokyo Bay. Bull. Jap. Soc. scient.
GROWTH RINGS IN BEAKS OF MOROTEUTHIS
la vida del calamar hay muy poco desgaste de la punta rostral en las serie de tama-
fios estudiados (longitud rostral 0.7-2.0 cm). Los histogramas de frecuencia y las
medidas del nümero de microanillos en cada ciclo muestran que estos no pueden
formarse por fortuitas fluctuaciones de secreción, aún cuando esas fluctuaciones
representaran la influencia de ciclostardios que son mäs estrechos que los tempranos.
El crecimiento del pico puede ser expresado convenientemente como un aumento en
la longitud de la pared, que es la distancia desde la punta rostral al ängulo antero-
interior de la pared lateral (Fig. 2). Desde que la historia del crecimento se registra
por la distancia que separa los microanillos desde la punta rostral, esta puede calcu-
larse retroactivamente. Aumento en tamafio del pico junto con al aumento en el
numero de ciclos ha sido diagramada, asi como la curva del calculo retractivo no
sujeta a ninguna parcialidad selectiva por el cachalote, (Fig. 8). El calculo de la
longitud de las paredes de los picos de mucha edad da valores mas bajos que los de
los jóvenes, probablemente porque los calamares de desarrollo más lento sobreviven
más tiempo. La relación entre la longitud de la pares y tamaño del calamar también
se ha diagramado (Fig. 10,11). El tiempoque toma la secreción de un ciclo no ha sido
establecida, pero ensayos basados en previos estudios sobre otros cefalópodos,
sugiere de 6 a 12 meses.
307
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MALACOLOGIA, 1966, 3(3): 309-325
THE CHROMOSOME CYCLE IN THE LAND SNAIL
CATINELLA VERMETA (STYLOMMATOPHORA: SUCCINEIDAE)!;2
C.M. Patterson and J. B. Burch
Museum and Department of Zoology
University of Michigan, Ann Arbor, Michigan, U.S. A.
ABSTRACT
At least 3 members of the genus Catinella are unique among the Stylommato-
phora because of their low chromosome numbers (C. rotundata of Hawaii, n=5
(2n=10); С. vermeta and С. texana, n=6 (2n=12)). Because of this low number
and relatively large size of the chromosomes, C. vermeta is particularly well
suited for a study of the chromosome cycle during spermatogenesis.
The cycle does not differ, in general, from that found in other animals, and
especially resembles the cycle we have observed in other euthyneuran snails. De-
tails, however, are much clearer, the various stages more easily recognized,
and those not detected with certainty before are now clearly evident. The de-
tailed description of the chromosome cycle of C. vermeta gives a clear concept
of the meiotic process in euthyneuran gastropods and expands greatly on infor-
mation contained in any previous report.
Early mitotic chromosomes appear as fuzzy, diffuse strands which condense
to form mid-prophase chromosomes, the coilednature of which is evident; the
centromeres appear as lightly stained or nonstained areas. Further contraction
results in metaphase chromosomes that stain more densely, have smooth
margins and centromeres indicated only by constrictions. Anaphase chromo-
somes are similar but somewhat smaller.
The first meiotic prophase nucleus is formed after the last pre-meiotic di-
vision. The leptotene chromosomes appear as lightly stained, long, single
strands with chromomeres along their length. The free ends show the polari-
zation characteristic of the “bouquet stage”. Zygotene pairing begins at the
polarized ends and appears to be chromomere-by-chromomere along the length
of the homologous strands. Pachytene chromosomes are shorter and more
densely stained. Homologues begin to “repel” one another, causing a separation
that produces open areas along early diplotene chromosomes. As diplonema
progresses, the chromosomes become diffuse and poorly stained. Chiasmata
terminalize and contraction continues as the chromosomes form the ring, rod,
cross or multiple loop-shaped figures characteristic of diakinesis. Metaphase I
bivalents are very condensed ring, half-ring or rod-shaped figures in polar
view. Homologous centromeres, with their chromatids, separate at Anaphase I,
forming dyad chromosomes about 1/2 the size of Metaphase I bivalents. Fol-
lowing cytokinesis, the chromosomes enter the 2nd meiotic division without an
observable period of interkinesis.
Prometaphase II dyads, before alignment in the equatorial plane, look like
later Metaphase II chromosomes, which are greatly contracted, densely stained
1
Contribution from the University of Michigan Biological Station.
2 This investigation was supported (in part) by research grants GB 787 from the National Science
Foundation, Washington, D.C., U. S. A., 5 T1 AI 41-07 from the National Institute of Allergy
and Infectious Diseases, U.S. Public Health Service, and by a Public Health Service research
career program award (number 5-K3-AI-19, 451-03) to the second author.
(309)
310 PATTERSON AND BURCH
and “dumb-bell” shaped.
During Anaphase II, each dyad separates to form 2
monads, which pass to opposite poles, where Telophase II is initiated and sub-
sequent cytokinesis takes place.
Young spermatids are then formed, each
having a conspicuous nuclear membrane. During spermiogenesis, thechromatin
becomes disorganized and nuclear condensation takes place to form the mature
spermatozoa.
INTRODUCTION
Land snails of the genus Catinella
have recently evoked considerable
interest from the cytological point of
view because of the unusually low
chromosome numbers of at least 3 of
its species (n=5, 2n=10 in C. rotundata
(Gould) of Hawaii and n=6, 2n=12 inC.
vermeta (Say) and C. texana Hubricht of
continental U. S. A.) (Burch, 1964a, b;
Burch & Patterson, 1965). Having such
low numbers, these species are particu-
larly well suited for a complete study
of the chromosome cycle. The present
paper deals with the cytological aspects
of C. vermeta and includes an analysis
of the chromatin throughout the chromo-
some cycle during spermatogenesis and
spermiogenesis as well as a description
of several chromosomal anomalies
sometimes occurring during the cycle.
The description ofthe chromosome cycle
in C. vermeta gives a clear. Concept of
the meiotic process in euthyneuran
gastropods and expands greatly on in-
formation contained in any previous
reports.
Catinella vermeta is common to much
of the United States. Its generalized
distribution, as currently known, is
shown in Fig. 1. Its actual distribution
may well cover the entire continental
U.S. А., but lack of collecting in certain
geographical areas and the past nomen-
clatural and taxonomic confusion in
regard to succineid snails makes
accurate tabulations from the literature
difficult.
The species that is now understood to
be Catinella vermeta (Say, 1824b) has
been commonly known in the past as C.
(or “Succinea”) vagans (Pilsbry) (see
Pilsbry, 1948; Miles, 1958; Burch,
1962). Hubricht (1961) found that the
FIG. 1. Distribution of Catinella vermeta.
type lot of Succinea campestris vagans
Pilsbry, 1900, contained a mixture of 2
species which, on shell characters, could
not be distinguished from S. campestris
Say and C. vermeta (Say). The original
description of S. vagans was based on
the shells of S. campestris. In addition,
the species which until recently has
been referred to as “C. (or Succinea)
avara (Say)” is probably none other than
C. vermeta. Say’s (1824a) type speci-
men for “Succinea avara” is animmature
shell and unidentifiable (Hubricht, 1958).
Catinella vermeta inhabits moist
places, usually near bodies of fresh-
water, and can be found crawling on the
surface of the ground, or resting under
wood, leaves or stones. Its shell is
characteristically covered with moist
mud. C. vermeta may be distinguished
from neighboring succineids of the
genera Succinea and Oxyloma partly by
characters of its shell, but more surely
by the lack of a penial sheath, which is
present in the other 2 genera. So far
as known, species of Succinea and Oxy-
CHROMOSOME CYCLE IN CATINELLA 311
loma all have higher chromosome
numbers (n=15 or more), which makes
them less ideal for a study of the chromo-
some cycle.
LITERATURE REVIEW
The maincomprehensive publications
on chromosomes of euthyneuran Gastro-
poda are those of J.-L. Perrot (1930),
M. Perrot (1938), Inaba (1959a, b), Husted
& Burch (1946) and Burch (1960a, b).
These and other papers dealing with
cytology in Euthyneura are summarized
by Burch (1965). J.-L. Perrot (1930)
studied the formation of germinal cells
and the chromosome cycle during
spermatogenesis in a basommatophoran
and a stylommatophoran snail; he also
studied the “heterochromosomes” in
several Stylommatophora and discussed
chromosome numbers reported in pul-
monate snails. M. Perrot (1938) deter-
mined the chromosome numbers in 17
species of Stylommatophora and dis-
cussed snail taxonomy in relation to
those numbers. Inaba (1959a) studied
the chromosomes of 29 species of the
Stylommatophora and related these num-
bers to present systematics. He also
determined the chromosome numbers of
19 species of opisthobranchiate mol-
lusks (1959b), discussing higher system-
atics in relation to his observations.
Husted & Burch (1946) examined the
chromosomes of 18 species and sub-
Species of the stylommatophoran family
Polygyridae; they studied 1 populationin
particular regard to varying chromo-
some numbers and heteromorphic biva-
lents, and discussed chromosome num-
bers of the “Pulmonata” in general.
Burch (1960a) studied the mitotic chro-
mosomes in 5 families of the Basomma-
tophora and discussed the value of karyo-
type analysis and chromosome numbers
to snail systematics. He further in-
vestigated the chromosomes of 36 spe-
cies and subspecies of basommatophoran
snails, reviewed all previous work on that
group, discussed taxonomy in relationto
chromosomes, and studied formation of
germ cells and the chromosome cycle
during spermatogenesis of 1 species
(Burch, 1960b).
Previous authors that have discussed
within the last 25 years the chromosome
cycle of euthyneuran gastropods are
J.-L. Perrot (1930: Lymnaea stagnalis,
Lehmannia marginata; 1937: Helx
pomatia), Pennypacker (1930: Polygyra
[=Mesodon] appressa), Hickman (1931:
Succinea ovalis), Whitney (1941: Vallon-
ia pulchella), Tuzet (1951: Physa acuta),
and Burch (1960b: Stagnicola emar-
ата). All of the observations by
those authors, with the exception of the
description on 5. emarginata, were from
sectioned material, a method which is
inferior to the squash technique. Because
of its much higher chromosome number
(n=18), S. emarginata is not as satis-
factory an animal to study as Catinella
vermeta (n=6), the species used in this
paper.
Previous papers which have treated
in one way or another the chromosomes
of Succineidae, to which Catinella ver-
meta belongs, are those by Hickman
(1931), M. Perrot (1937, 1938), Inaba
(1945, 1950, 1959a), Husted & Burch
(1946), Koyama (1955), Burch (1964a, b)
and Burch & Patterson (1965). Hick-
man’s paper deals with the spermio-
genesis of Succinea ovalis from the
U. S. A., including formation of germ
cells, the chromosome cycle, cyto-
plasmic inclusions and sperm formation.
Perrot gave the haploid chromosome
number of S. putris (n=22). Inaba (1945,
1950) gave the haploid and diploid
numbers of $. horticola (n=17, 2n=34)
and in (1959a) described the mitotic
and meiotic metaphase chromosomes of
that species. In the latter paper he
also discussed aspects of cytotaxonomy
in the Succineidae. Husted & Burch,
in a footnote to their polygyrid paper,
gave the chromosome number of S. ova-
lis (n=21) from Virginia, U. S. A., and
noted that their findings differed from
Hickman’s (n=20) report for the same
Species from Maine and New Jersey.
Koyama gave the haploid and diploid
numbers of S. hirasei and 5. kwansae
(both with n=17, 2n=34), briefly described
312 PATTERSON AND BURCH
’ us bo
Pr.
DAA + q 7
FIGS. 2-7. Mitotic and meiotic chromosomes of spermatogenesis in Catinella vermeta. FIG.
2. Spermatogonial early prophase. Arrow indicates proper cell. FIG. 3. Spermatogonial mid-
prophase. Arrows denote centromeric regions. FIG. 4. Spermatogonial metaphase. 4a is
greatly magnified as shown by measurement line. The inset figure (4b) has the same magnifica-
tion as Figs. 2, 3, 5-7. The arrow points to a secondary constriction in one arm of one of the
largest chromosomes. FIG. 5. Spermatogonial anaphase. The arrows point to secondary con-
strictions in thelagging sister chromosome arms. FIG. 6. Pre-leptotene nucleus. FIG. 7. Four
leptotene nuclei.
All figures except 4a are magnified as shown in FIG. 5.
their meiotic and mitotic metaphase chromosome data were available. Burch
chromosomes and discussed cyto- (1964a, b) gave the chromosome numbers
taxonomy of succineid snails for which of Catinella vermeta (n=6, 2n=12) and
CHROMOSOME CYCLE IN CATINELLA 313
C. rotundata (n=5, 2n=10) and discussed
systematics in the family Succineidae
in the light of chromosome numbers.
Burch & Patterson (1965) pointed out
that the genus Catinella affords excellent
cytological material for demonstrating
and studying the chromosome cycle in
an animal.
MATERIALS AND METHODS
The specimens of Catinella vermeta
used in this study were collected from
4 locations in Michigan: the border of
a woods pool in central Washtenaw
County; a damp, marshy area adjacent
to the Raisin River near Clinton, northern
Lenawee County; the edge of the Raisin
River near Tecumseh, northern Lenawee
County; and the shore of Douglas Lake,
Cheboygan County. The specimens were
killed, fixed and preserved in New-
comer’s (1953) fluid prior to cytological
examination. Tissue of the ovotestis
was prepared for chromosome studies
by the acetic-orcein squash technique
(La Cour, 1941). Observations were
made with Nikon compound microscopes
using 100X (n.a. 1.25) oil immersion
objectives and 10X and 30X oculars.
The chromosomes were drawn with the
aid of a camera lucida and reproduced
at a table top magnification of 5340X.
Photomicrographs were taken using a
10X ocular, oil immersion objective,
a Kodak Wratten 57A (green) filter and
Kodak High Contrast Copy film.
OBSERVATIONS
Spermatogenesis in Catinella vermeta
consists of a number of spermatogonial
(mitotic) divisions of germ cells prior
to the maturational (meiotic) divisions.
The spermatogonial mitoses of C. ver-
meta appear to be characteristic of
normal somatic mitoses as they occur
in other animals with the diploid number
(2n) of chromosomes visible during the
divisions.
The chromosomes of early mitotic
prophase appear as rather fuzzy, diffuse
strands with extremely irregular mar-
gins (Fig. 2). The strands are long
with slightly darker staining sections
along their length. The 12 mitotic
chromosomes can be seen as distinct
entities and actually can be counted at
this early stage in favorable prepara-
tions. The mid-prophase chromosomes
(Fig. 3) are somewhat shorter, more
deeply stained and have smoother mar-
gins than those of early prophase as
a result of increased chromosome con-
traction. The coiled nature of the
strands is particularly evident at this
stage. The area of the centromere ap-
pears as a lightly stained or non-stained
portion of each strand and this area
produces the primary constriction ofthe
chromosome. All 12 chromosomes can
easily be counted. In late prophase
(Fig. 8), the chromosomes are even
more condensed, deeply stained, shorter
and have smoother margins than those
of mid-prophase. The coiled nature
of the strands and the differential staining
of the centromeric regions are not as
apparent because of the increased con-
traction. However, constrictions can be
¿>
Le
D |
FIG. 8. Spermatogonial late prophase chromo-
somes.
PATTERSON AND BURCH
У? 2> 32 >> ]) >>
10 u
FIG. 9. Spermatogonial metaphase chromosomes.
The homologous pairs have been arranged
in decreasing order of length.
seen to indicate the centric area in
some chromosomes. The 12 chromo-
somes can be distinguished with par-
ticular ease in this stage.
Metaphase chromosomes are greatly
contracted, deeply stained, have smooth
margins (Fig. 4a,b) and show no evidence
of coiled structure as they do in pro-
phase. The centromeric regions are
indicated only by constrictions which are
located at the “bend” of the chromo-
somes, where the centromereisattached
to the bi-polar spindle apparatus. The
karyotype of C. vermeta includes 1 pair
of conspicuously large chromosomes, 4
pairs which are intermediate in size
and 1 smaller pair (Fig. 9). All of
the chromosomes appear to be almost
medianly constricted (metacentric) but
several may be submedianly constricted
to a slight degree. A secondary con-
striction is clearly evident near the end
of an arm of one of the large chromo-
somes; it is probably present in its
homologue, but is not always as clear.
Spermatogonial metaphase chromo-
somes range in length from 5.6 u for
the largest pair to 3 y for the smallest
pair.
Anaphase chromosomes have much the
same shape and density of stain asthose
of the preceeding metaphase, but are
usually somewhat smaller. The chromo-
somes of the 2 anaphasic groups are
pulled from their centromeres toward
opposite poles and sometimes sister
chromosome arms may encounter diffi-
culty in separating and lag behind the
other chromosomes in the complement
(Fig. 5). The secondary constriction
on one of the largest chromosomes is
usually again evident in sister chromo-
some arms that lag in anaphase.
During telophase, the chromosomes
become more tightly grouped within the
nucleus and resemble a rather solidball
of chromatin. Cytokinesis follows and
results in the formation of 2 equivalent
daughter nuclei each with the diploid
complement of chromosomes.
After the last pre-meiotic division,
the nucleus enlarges to form the first
meiotic prophase nucleus. The pre-
leptotene nucleus (Fig. 6) contains
localized accumulations of chromatin
that are rather “granular” in appearance
and only partially formed into chromatin
strands. In leptonema (Fig. 7) the
chromosomes appear aS maximally ex-
tended single strands, which are lightly
stained, with more darkly stained bead-
like chromomeres along their length.
In late leptonema, the free ends of the
chromosomes’ are polarized, i.e.,
associated at one side of the nucleus,
forming the “bouquet stage”.
The pairing (synapsis) of homologous
chromosomes begins in zygonema. The
chromosomes begin to synapse at the
polarized ends, while the remainder of
the strands are yet unpaired in the
“bouquet” formation (Fig. 10). The
zygotene chromosomes appear to be
somewhat more contracted and darkly
stained than leptotene chromosomes and
the chromomeres are still clearly evi-
dent.
Pairing of homologous strands is com-
pleted in zygonema forming pachytene
chromosomes of double thickness and
haploid in number. The “bouquet” per-
sists into early pachynema and the
separate homologues can still be dis-
cerned (Fig. 11). Pairing seems to be
CHROMOSOME CYCLE IN CATINELLA 315
FIGS. 10-15. Meiotic prophase chromosomes of spermatogenesis in Catinella vermeta. FIG.
10. Zygonema. The arrows indicate synapsis at the polarized ends, while most of the rest of
the strands are not yet paired. FIG. 11. Pachytene bivalents. FIG. 12. Late pachytene bi-
valents. FIG. 13. Early diplonema. Arrows indicate places where the chromosomes are be-
ginning to “open out”. FIG. 14. Diplonema (diffuse stage). FIG. 15. Late diplonema.
All figures are magnified as shown in FIG. 13.
chromomere-by-chromomere along the creased contraction ofthe strands, which
length of the homologous strands. Late begins in leptonema and continues
pachytene chromosomes (bivalents) (Fig. throughout Prophase I. In favorable
12) are much shorter than leptotene or preparations, the 6 bivalents can be
zygotene chromosomes, due to the in- counted in late pachynema.
316 PATTERSON AND BURCH
10yu
FIG. 16. Camera lucida drawing of the paired ends of 6 of the zygotene chromosomes shown in
the photograph to the left and in Fig. 10. Strands partly or wholly out of the optical plane are not
shown.
In early diplonema (Fig. 13), the
homologues begin to “repel” one another,
causing the chromosomes to separate
slightly; but since they remain connected
at the points of crossing-over (chias-
mata), open areas or loops are formed
along their length. Early diplotene
chromosomes still stain rather deeply;
however, the chromosomes of mid to
late diplonema appear more diffuse,
poorly stained and with irregularly
characterized margins (Figs. 14, 15).
As terminalization of chiasmata begins
and contraction continues, the chromo-
somes soon form the ring, rod, cross
or multiple loop-shaped figures charac-
teristic of diakinesis (Figs. 17, 18). In
early diakinesis, the chromosomes are
still quite diffuse and have irregular
margins (Fig. 17). Due to the increased
contraction, mid to late diakinetic
chromosomes are smaller, more deeply
stained and have somewhat smoother
margins (Fig. 18). The shapes of the
various diakinesis bivalents that have
been observed in C. vermeta are shown
in Fig. 21 with arrows indicating
positions of the chiasmata. Cells in
which the 6 bivalents form 6 ring-shaped
figures (Fig. 21a, b, c) or 5 ring and 1
rod-shaped figure (Fig. 21d) occur in
about equal frequency and are most
common. Less frequently, 4 ring and
2 rod-shaped figures are observed and
occasionally cross and multiple loop-
shaped bivalents (Figs. 21е, resp. 211)
are present. Ring-shaped bivalents
have 2 remaining chiasmata and rod-
shaped figures presumably have 1
terminal chiasma remaining. Of the
other figures observed, the cross has 1
non-terminal chiasma and the multiple
loop has 3 remaining chiasmata, pro-
ducing 2 loops.
The continued contraction throughout
Prophase I forms Metaphase I bivalents
that are very condensed with deep stain
and smooth marginal outlines. The
bivalents form either ring, half-ring or
rod-shaped figures in polar view, de-
pending upon the number and location
of remaining chiasmata. Cells with 6
rings or those with 5 rings and 1 half-
ring are most frequently observed. Six
bivalents that range in size from 3.2-
2.3 u, measured at the greatest dimen-
Sion, are shown in Fig. 19.
Homologous centromeres, with their
chromatids of varying genic constitution,
separate at Anaphase I and the dyads
move toward opposite poles. Fig. 20
clearly shows the monocentric nature of
CHROMOSOME CYCLE IN CATINELLA
19
<
4
20
FIGS. 17-20. Meiotic chromosomes of spermatogenesis in Catinella vermeta. FIG. 17. Early
diakinesis bivalents. FIG. 18. Late diakinesis showing 6 ring-shaped bivalents.
FIG. 20. Metaphase-Anaphase I bivalents in side view.
phase I bivalents.
FIG. 19. Meta-
All figures are at the magnification shown in Fig. 18.
the chromosomes as the 2 halves of
each bivalent are just beginning to be
pulled apart. The chromosomes in each
anaphasic group are about 1/2 the size
of Metaphase I bivalents, but density
of stain and smoothness in outline are
much the same. The centromeric
regions of the dyads can be seen as
constrictions in some chromosomes and
may appear more lightly stained. Two
dyad members of a bivalent are some-
times late in separating and they there-
fore lag in the center of the cell after
the other dyads have passed to their
respective poles. A cell in this con-
dition is shown in Fig. 22. Cytokinesis
follows and spindle formation takes
place as the chromosomes seem to
immediately enter the second meiotic
division without undergoing an obser-
vable period of interkinesis (Fig. 23).
During Prometaphase II spindle for-
mation is completed and the dyads begin
to move toward the equator of the cell
(Fig. 23). The dyads appear to be
just as highly contracted, or even more
so, as in the previous anaphase. Cen-
tromeric regions are indicated only by
constrictions, with no evidence of dif-
ferential staining. Fig. 24 shows Meta-
phase П dyads which appear as single
or double “dumb-bell” shaped figures
with the centromeric constrictions
clearly evident. The chromosomes of
Metaphase I are highly contracted,
deeply stained and have smooth mar-
ginal outlines. Six dyads are easily
counted, with the largest and smallest
of the complement measuring 2.6 u
and 2.1 y respectively in length, thus
318 PATTERSON AND BURCH
oa 3
* +
еее
10 u
FIG. 21. Diakinesis bivalents of Catinella vermeta. 21a-c, Ring-shaped bivalents, each with 2
chiasmata. 21d, Rod-shaped bivalent with 1 terminal chiasma. 21е, Cross-shaped bivalent
with 1 non-terminal chiasma. 21f, Multiple loop-shaped bivalent with 3 chiasmata. Arrows in-
dicate positions of chiasmata.
being smaller than the Metaphase I bi-
valents.
In Anaphase Il, each dyad separates
to form 2 monads or daughter chromo-
somes, which pass to opposite poles.
The Anaphase II chromosomes often
appear to have slightly more irregular
margins than Metaphase II dyads. The
6 separating dyads of early Anaphase
II are easily counted in Fig. 25, where
1 dyad can be seen to be noticeably
larger.
When the chromosomes reach their
respective poles, Telophase I is ini-
tiated and cytokinesis begins to take
place (Fig. 26). Thehaploid complement
now consists of 1 large chromosome
and 5 smaller chromosomes randomly
oriented within the nucleus. In late
Telophase II (Fig. 27), the chromosomes
are often grouped together near the pole,
appearing as a solid mass of chromatin.
Upon completion of Telophase II and cyto-
kinesis, the chromosomes pass into an
interphasic-like state, the chromatin
characteristically becoming somewhat
diffuse and irregular in shape. Thus
begins the formation of young sperma-
tids, each with its conspicuous nuclear
membrane (Fig. 28). All 6 irregularly
Shaped chromatin masses can still be
clearly discerned in some of the young
CHROMOSOME CYCLE IN CATINELLA 319
26 | 27. *
FIGS. 22-27. Meiotic chromosomes of spermatogenesis in Catinella vermeta. FIG. 22. Late
Anaphase I. Two dyads, both from the same bivalent, are at the center of the cell; they ap-
parently had difficulty in terminalizing, and therefore lagged behind the other dyads in their
anaphasic movement. FIG. 23. Prometaphase II dyads in 2 sister cells. FIG. 24. Metaphase II
dyads (note spindle fibers). FIG. 25. Metaphase-Anaphase II dyads. FIG. 26. Telophase II
monads in 2 sister cells. FIG. 27. Late Telophase II.
All figures are at the magnification shown in Fig. 25.
spermatids. During spermiogenesis, the deeply stained, nearly mature sperm
chromatin becomes progressively more cells are formed (Fig. 31). The mature
disorganized and nuclear condensation sperm head measures 2.5 „ in diameter
occurs (Figs. 29, 30), until very small, and is about 1/3 the size of the young
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MALACOLOGIA, 1965, 3(3): 327-378
REPRODUCTIVE FUNCTION AND THE PHYLOGENY
OF OPISTHOBRANCH GASTROPODS
Michael T. Ghiselinl
ABSTRACT
The comparative and functional anatomy of the reproductive system through-
out the subclass Opisthobranchia is treated critically to provide a sounder basis
for phylogenetic studies. Original observations are combined with detailed dis-
cussions of older work. Emphasis is given to possible functional explanations
for morphological and physiological variations, in order to allow a phylogenetic
theory which has a causal theoretical basis. Functional analysis is employed,
involving the avoidance of features likely to be convergent, and emphasizing
comparison based on complex functional divergences.
Homologies of the parts are treated in detail, and some changes in nomen-
clature are suggested. The formation of egg masses and the homologies of the
glands which secrete them are discussed and clarified by histochemistry and ex-
perimental observations.
Possible reasons for evolutionary changes are considered. Functional dis-
advantages of the ancestral, undivided gonoduct have been overcome in different
ways, and these divergences form the basis of hypothetical clades which are
evaluated in terms of other evidence.
The study considers older systematic work, chromosome numbers, feeding
. specializations and other properties of the digestive system, and spermatozoon
morphology as auxiliary evidence in adiscussion of phylogenetic problems. The
phylogenetic arguments incorporate critical consideration of parallelism and
convergence.
The reproductive system in the Onchidiidae supports pulmonate affinities.v
The Acteonidae have a modified reproductive system and are not ancestral to
most other opisthobranchs; the reproductive system and some other structures
imply a close relationship to the Hydatinidae; the histology of the ampulla
suggests a possible affinity to the Acoela. The premises on which arguments
for abiphyletic origin of pteropods have been based are rejected; a monophyletic
origin is consistent with the morphology of the reproductive system; both groups
resemble the Anaspidea and Sacoglossa in spermatozoon morphology. The re-
productive systems of Anaspidea, Sacoglossa, Diaphanidae and Cylindrobullidae
can be compared to a hypothetical common ancestor with a divided gonoduct, and
may be related. The Retusidae, Philinoglossidae, Bullidae, Atyidae and Runcin-
idae may be grouped together onthe basis of a copulatory apparatus which stores
sperm and forms spermatophores; herbivorous members of this group have an
oesophageal diverticulum and similarities in the gizzard. Correlations between
larval shell types and the triaulic condition in aeolid nudibranchs suggest some
need for systematic revision. The study supports the naturalness of many
groups.
INTRODUCTION there being no wholly satisfactory,
natural system of classification. Recent
The relationships within the subclass work has provided new evidence bearing
Opisthobranchia are most uncertain, on systematic problems, but there has
lHopkins Marine Station of Stanford University, Pacific Grove, California; present address:
Museum of Comparative Zoology, Harvard University, Cambridge 38, Massachusetts, U. S. A.
(327)
328
been no adequate, comprehensive syn-
thesis. This study aims ata contribution
to such a synthesis, and at a recon-
sideration of older phylogenetic ideas in
the light of more modern evolutionary
concepts. Ideally, a phylogenetic study
should treat all the relevant evidence;
but this is difficult, and attempts to do so
often lead to superficial comparisons.
Therefore a particular organ system is
here treated in detail, and phylogenetic
hypotheses are formulated on the basis
of this comparison. An effort is then
made to see how well the hypotheses
agree with inferences made from other
kinds of evidence, especially with the re-
sults of recent work. Like any other phy-
logenetic study, this body oftheory is de-
signed to serve as abasis for further re-
search by providing hypotheses which
may be tested by critical work, especially
on other systems. Itis not intended as the
final word on relationships, but only as
the implications of a particular, limited
perspective, which may be interestingto
those who desire to further our under-
standing of opisthobranch phylogeny.
This study has been based on a tech-
nique which departs somewhat from the
usual approach, and some discussion is
essential to an understanding of the argu-
ments which follow. Functional analysis
has been applied in order to take the
causes of evolutionary change into
account in reconstructing the sequences
of modification. The comparison is
organized in terms of physiology in the
broad sense, since this approach allows
the selection of properties of the
organism for comparison on the basis of
biological significance rather than con-
spicuousness or convenience. I reject
the purely morphological approach, since
it is likely to confuse non-adaptive
characteristics with those the adaptive
Significance of which is not known, and
rather choose to begin with con-
Siderations of adaptive significance.
This approach has value too, in the
light it casts on physiology, in that
morphological variations may suggest
correlated physiological ones.
M. T. GHISELIN
The difficulty in classifying opistho-
branchs results in part from extreme
modification, and also. from the great
amount of parallelism and convergence
which characterizes the group аз a whole.
The opisthobranchs are in the process
of losing the shell. Correlated with this
loss of the shell are various other
changes in structure, including the re-
organization of the body into a slug-
like organism with a modified respira-
tory apparatus, concentrated nervous
system and bilateral symmetry. Morton
(1963) refers to this reorganization and
the shifts of adaptive zone which it
allows as a “program” evolution, and
points out that the changes are poly-
phyletic. In order to avoid being led
astray by parallelism and convergence,
I have incorporated a consideration of
the possible causes of these compli-
cations into the theoretical perspective
which is used. In this work I shall refer
to a selective influence as any cause of
selection pressure. Itake Ц аз axiomatic
that parallelism and convergence are
caused, fundamentally, by the action of
the same selective influence, and that
wherever the same selective influence
acts on organisms, parallelism and con-
vergence are likely. (The difference
between parallel and convergent evo-
lution is largely a matter of degree, the
distinction simply emphasizing the
greater propensity of closely-related
organisms to undergo particular kinds
of changes under the same conditions.)
In study of long-term evolutionary change
especially, it is desirable to base com-
parison on changes which have an un-
equivocal functional advantage, since to
do so allows reasonable grounds for
assuming that evolution has tended to
proceed in a particular direction. But
just because of such advantage, parallel-
ism is likely in closely-related forms.
Therefore, in evaluating phylogenetic
hypotheses, I avoid drawing the con-
clusion that organisms showing identical
structure are related if that similarity
can readily be explained in terms of
convergence resulting from such in-
PHYLOGENY OF OPISTHOBRANCHS 329
fluences as may reasonably be supposed
to have produced them. Rather, the
attempt is made to erect a coherent
system of relationships based as much
as possible on differences which have
explanatory value as divergent adap-
tations to the same selective influence.
These differences, which Bock (1959)
speaks of as multiple pathways of adap-
tation, are indications of earlier con-
ditions in which a particular functional
problem still existed. Although it is not
strictly true, it is here assumed, with
reservations, that the reproductive
system evolves relatively independently
of other systems, hence that its own
convergences and parallelisms are in-
dependent of those of other systems,
and that independent correlation should
obviate some of the problems of paral-
lelism. Further, in a complex organ
system it seems reasonable to assume
that identical complex structures are not
convergent if a variety of functional
arrangements can provide improvement
over antecedent conditions; however,
there are numerous logical pitfalls in
the evaluation of phylogenetic hypotheses
in this light. For instance, it is very
easy to confuse lack of evidence for a
hypothesis with evidence against it, as
when there has been a secondary loss
of a structure. Such practical compli-
cations of reasoning must be dealt with
individually.
A causal phylogenetic system is an
attempt at explanation which, because it
does explain, may be evaluated by the
implications of the explanations it gives.
It is argued in this study that some of
the variations of the reproductive system
are understandable in terms of
physiology. Of course, our ability to go
so far as to make precise predictions
of the course of evolution is made im-
possible by unknown selective influences,
random changes and pleiotropy. Butthis
does not mean that we cannot use our
understanding of physiology or evolution-
ary mechanisms as evidence for or
against a particular relationship. Itis
one thing to make a prediction con-
cerning the course of evolution, another
to recognize that its regularities impose
restrictions and tendencies upon evo-
lutionary history such that certainhypo-
thesis are more credible than others.
Thus, ifa particular phylogenetic scheme
places the various forms in a pattern of
sequences such that the transitions have
explanatory value as adaptations and the
changes are by gradual, adaptive steps,
then the system is supported. Similarly,
a system in which the changes can only
be explained by macromutations or ad
hoc rationalizations is relatively un-
satisfactory. One cannot, by comparative
anatomy alone, prove that phylogenetic
theories are true. However, one can
disprove them in a sense by forming
hypotheses based on independent struc-
tures and rejecting the hypotheses when
they contradict each other. Thus a
phylogenetic system is not alone that
which is best supported, but that which
best withstands criticism.
The particular kinds of selective in-
fluences which are thought to act upon
a group and the conditions which are
hypothesized as ancestral, determine the
kind of arguments which are valid in
support of a particular system. For
instance, Boettger (1954) erected a
phylogenetic system of the euthyneurous
gastropods on the degree of development
of the following: (1) detorsion of the
visceral loop, (2) shortening of visceral
connectives, (3) fusion of ganglia, (4)
position of the pharyngeal nerve ring
relative to the pharynx, (5) loss of the
shell, (6) loss of the operculum. As
stated above, I agree with Morton (1963),
and with Pelseneer (1894), Fretter &
Graham (1962) and others in believing
that these changes tend to be polyphyletic.
There can be no reasonable doubt that
loss of the shell has occurred inde-
pendently within numerous clades
(Hoffmann, 1932-40). Loss of the oper-
culum probably results from loss of
protective significance ofthe shell. Con-
centration of the nervous system and
detorsion correlate to a considerable
degree with the loss of the shell, andare
330 M. T. GHISELIN
also known to be polyphyletic. I demon-
strate below that Boettger’s inferred
relationships are not valid unless some
parallelism is admitted. From the poly-
phyletic nature of these changes it follows
that there is no way to determine at
what stage of their evolution the various
lines of descent diverged, except toinfer
that the common ancestor ofa particular
group was as primitive in the develop-
ment of a trend as the most primitive
known member. Therefore Boettger’s
criteria are such that they are likely to
result in Stufenreihe rather than Ahnen-
reihe. I do, however, accept Boettger’s
criteria in so far as they employ
divergences inthe nervous system rather
than stages in trends. Therelationships
suggested by this study are supportedby
such differences.
Another problem of convergence re-
sults from small size. The convergences
of small organisms are well known
(Rensch, 1960). They may be under-
stood by consideration of their adaptive
Significance. In general, organisms
undergo changes during the reduction of
body size which result in a saving of
space, such as simplification of compli-
cated structures, loss of less essential
parts, and concentration of.the nervous
system. They also show such changes
as development of ciliary locomotion and
reduction in the relative surface of the
gill which have an obvious physiological
explanation. Such superficial conver-
gences are compensated for as a matter
of course; however, sometimes the adap-
tive significance of a particular modifi-
cation is overlooked. For instance,
protandry may be advantageous in small
opisthobranchs because it saves space;
but it also may be primitive in the group;
in a small, protandrous form, it may be
hard to tell whether the protandry is
primitive or secondary.
From such considerations, one may
avoid being led astray by convergence
simply by avoiding conclusions from
Similarities which, within a given con-
text, are particularly likely to be con-
vergent.
This study has involved a detailed
critique of the literature, as well as
observations on the organisms them-
selves. Particular emphasis is given to
physiology as the basis of comparison.
It has been necessary to evaluate the
literature, particularly where conflicts
and lacunae exist. Various uncertain-
ties must, of course, be resolved by new
research before the results of this study
can be properly tested. I have tried
to give proper credit to those who have
originated the ideas which are developed
here; however, this has been complicated
by the fact that the advancement of phylo-
genetic knowledge comes more from cor-
relating and evaluating the data than from
unearthing similarities and differences.
Therefore, it may be that adequate cre-
dit has not been given to everyone whose
work has been useful.
I have attempted to cover the relevant
literature, although this should not be
considered an exhaustive review, as only
matters relevant to the discussion are
treated here. For the older literature
Keferstein’s “Bronn” (1862-66) is useful,
and Pruvot-Fol (1960) discusses some
aspects of the reproductive system
throughout the group. The general
anatomy of the opisthobranchs is re-
viewed in Hoffmann’s “Bronn” (1932-
40), but this work does not include the
reproductive system.
To avoid involvement in nomenclatural
problems, the most widely-used names
are given. On the whole I have followed
the usage of Taylor & Sohl (1962),
except that the Acoela of Thiele (1929-
35) are retained.
METHODS
For dissection, animals were anaes-
thetized in aqueous magnesium chloride
solution isotonic with seawater. Egg
masses were fixed in buffered seawater
formalin to avoid hydrolysis of the
carbohydrates. Tissues used in histo-
logical and microanatomical work were
fixed in seawater Bouin’s solution, im-
bedded in paraffin and sectioned at a
PHYLOGENY OF OPISTHOBRANCHS 331
thickness of ca. 10 micra. The staining
techniques used, with their standard
abbreviations, were as follows:
Alcian Blue 8GX (AB) by the method
of Steedman (Pearse, 1961).
Azure A by the method of Kramer &
Windrum (1955).
Delafield’s acid haematoxylin.
Dimethylaminobenzaldehyde-nitrite
(DMAB) method of Adams for tryptophan
(Pearse, 1961).
Eosin Y in 95% ethanol.
Hale’s dialysed iron method for acid
mucopolysaccharides (Pearse, 1961).
Lasky’s Mucihaematin (Casselman,
1959).
The Mercury-Bromphenol Blue
(HgBPB) method of Mazia, Brewer &
Alfert (1953), using an aqueous solution,
for proteins.
Millon’s reaction (Bensley and Gersh
modification) for tyrosine (Pearse,
1961).
Periodic acid-Schiff (PAS) reaction by
the method of McManus (Pearse, 1961).
GENERAL STRUCTURE,
HOMOLOGIES AND NOMENCLATURE
The following is a description of an
idealized, gonochoric reproductive sys-
tem of such a structure that it may
serve as an hypothetical ancestral form;
it incorporates a uniform terminology
and a discussion of criteria of homolgy.
The variations will be discussed in later
sections. An attempt is made to utilize
terms which are consistent with Hyman’s
(1951) nomenclature for the Bilateria
in general, and with that of Fretter €
Graham (1962) for the Prosobranchia.
The functional morphology of the repro-
ductive system in the Prosobranchia,
from which the Opisthobranchia are
thought to be descended, has been dis-
cussed at length by Fretter & Graham
(1962), and such material will not be
repeated here.
Such an idealized, gonochoric system
is diagrammed in Figs. 1A and 1B. In
both the male and the female systems,
2 parts, the gonad and the gonoduct may
be distinguished. The male also has a
group of accessory structures. The
gonoduct (go) is divisible in both sexes
into 2 portions, the coelomic gonoduct
(co) and the pallial gonoduct (pl), terms
derived from the evident homologies of
these parts (Fretter & Graham, 1962).
Although the coelomic gonoduct in the
female is simple, and needs no further
terminology, that of the male is compli-
cated by the presence of a swelling, the
ampulla (am), which stores sperm before
they are transferred to the partner in
copulation. The term “hermaphroditic
ampulla” will not be used here because it
would be redundant. The ampulla is
often called the “seminal vesicle,” but
as this term is applied to a variety of
structures, its use is likely to be con-
fusing. When it is necessary to dis-
tinguish between the part of the coelomic
gonoduct lying between the gonad andthe
ampulla and that between the ampulla
and the pallial gonoduct, I will use the
terms pre-ampullar coelomic gonoduct
(pa) and post-ampullar coelomic gono-
duct (po) respectively. The use of such
terms as “hermaphroditic duct,” “little
hermaphroditic duct” and “largeherma-
phroditic duct” is avoided because of
their imprecision.
The pallial gonoduct in the male con-
sists of the prostate (pr) only. This
structure evidently plays some role in
the transfer of sperm, but its function
is poorly known. Chambers (1934) says
that it forms a kind of spermatophore, and
spermatophore formation by this struc-
ture is known in Haminoea (Perrier &
Fischer, 1914) and in Runcina (Ghiselin,
1963). A characteristic type of se-
cretory cell, the presence of which
seems to be a fundamental character of
the opisthobranch and pulmonate system,
occurs in the prostate of a wide variety
of euthyneurous gastropods. These cells
seem to have originally been pallial in
position, but they may be displaced to
the base of the penisinmanyforms. The
secretion of this cell may be recognized
by its corpuscular structure, and by its
staining reactions; in the literature,
332, 1 М. T. GHISELIN
go
FIG. 1. Idealized diagrams showing terminology. A, male system ina gonochoric form; B,
female system ina gonochoric form; C, hermaphroditic system suggestive of conditions in the
opisthobranch common ancestor.
al, “albumen” gland; am, ampulla; bc, bursa copulatrix; ca, copulatory apparatus; cg,
common genital opening; co, coelomic portion of the gonoduct; gd, gonad; go, gonoduct; me,
membrane gland; mu, mucous gland; ov, ovary; pa, pre-ampullar portion of the coelomic
gonoduct; pl, pallial portion of the gonoduct; po, post-ampullar portion of the coelomic gono-
duct; pr, prostate; rs, receptaculum seminis; sg, seminal groove; te, testis.
PHYLOGENY OF OPISTHOBRANCHS 333
the strong eosinophily of the secretion
is frequently noted. The eosinophilic
secretion may be accompanied by other
kinds of secretion. In order to extend
our knowledge of the chemical nature of
this secretion, I subjected formalin-
fixed sections of the prostate of a dorid
nudibranch, Triopha carpenteri Stearns,
and of a thecosomatous pteropod, Creseis
virgula Rang, toa series of histochemical
tests. The corpuscular secretion stained
deeply with eosin and very weakly with
haematoxylin; it did not stain at all with
AB or PAS; the DMAB reaction was
positive. Thus the secretion is probably
largely protein, and contains little, ifany,
carbohydrate. The prostate is probably
homologous throughout the group, but
more work is desirable.
The copulatory apparatus (ca) consists
of a penis with a ciliated groove which
extends to the pallial gonoduct. This
ciliated groove, or seminal groove (sg)
transports the sperm. Numerous modi-
fications of the copulatory apparatus have
been described. Where the open Seminal
groove has been converted into a closed
tube, it is called the vas deferens.
That portion of the vas deferens which
serves to transfer sperm through the
penis may be called the ejaculatory duct.
A swelling of the vas deferens which
forces sperm through the ejaculatory
duct will be called the ejaculatory
vesicle, The copulatory apparatus may
include a structure which stores sperma-
tozoa and which, in some forms atleast,
is associated with the production of
packets of sperm called spermatophores.
Although this structure is often called a
“male seminal vesicle,” this term may
be confused with any of several other
“seminal vesicles” and for this reason
the term spermatic bulb will be used.
The penis is often enclosed in a pro-
tective penial sac.
In the female, the pallial gonoduct in-
cludes sperm-containing structures and
secretory organs. There are usually 2
sperm-containing structures in the
pallial gonoduct. One of these, the
bursa copulatrix (bc) ordinarily receives
the sperm at copulation. The other, the
receptaculum seminis (rs), stores sperm
for longer periods. Common synonyms
for these structures are, respectively,
“spermatheca” and “spermatocyst.” The
most reliable criterion for distinguishing
between them is thatinthe receptaculum
seminis sperm may be found with their
heads attached to the epithelium (Fretter
& Graham, 1962; Pruvot-Fol, 1960).
Usually, but by no means always, the
receptaculum seminis occupies a
proximal position in the pallial gonoduct,
near the end of the coelomic gonoduct,
while the bursa copulatrix opens near
the opening of the pallial gonoduct to the
exterior. The contents of the various
sperm-containing organs are usually
given such circumlocutory or obscure
designations as “the animal’s own
Sperm”, or “ ‘foreign’ sperm.” The
terms endogenous and exogenous seem
preferable, since their meaning is clear
from the etymology.
In prosobranchs (Fretter & Graham,
1962), the receptaculum seminis and
bursa copulatrix are somewhat more
variable in structure and function than
in opisthobranchs, but generally the
bursa copulatrix receives the sperm and
the receptaculum seminis stores it.
Occasionally there is also an ingesting
gland which absorbs sperm; no homo-
logue of this structure has been re-
ported from the opisthobranchs. The
prosobranch receptaculum seminis
(Fretter € Graham, 1962) agrees with
that of the opisthobranchs (Lloyd, 1952)
in having an epithelium in which the
heads of the sperm become imbedded.
Fretter and Graham point out that “orien-
tation” of the sperm may occur ша
variety of parts of the gonoduct. The
bursa copulatrix ofprosobranchsis often
found to contain sperm and prostatic
secretion, but in some, the receptacu-
lum seminis is thought to also contain
both sperm and prostatic secretion
(Fretter & Graham, 1962). The bursa
copulatrix in prosobranchs is secre-
tory, and amoebocytes may ingest ma-
terials (Fretter € Graham, 1962); it is
334 M. T. GHISELIN
likewise secretory in opisthobranchs
(Foderä, 1915). Lloyd (1952) suggests
that the bursa copulatrix is fairly uni-
form in histology among opisthobranchs.
The uptake of materials by amoebocytes
in the bursa copulatrix is known in
prosobranchs (Fretter & Graham, 1962)
and Lemche (1956) thinks that the sole
function of the bursa copulatrixin Cylich-
na, a cephalaspidean, is the resorption
of prostatic secretion and materials
which go astray inthe reproductive tract.
Lemche’s interpretation is based partly
on his finding eggs in the bursa copula-
trix, partly by comparison with the ex-
perimental demonstration of Eales (1921)
that the exogenous sperm in Aplysia are
not deposited in the bursa copulatrix,
but rather near the base of the duct of
the receptaculum seminis. But this has
not been established by direct evidence.
In Aglaja and Runcina (Ghiselin, 1963)
I have observed that sperm are de-
posited just inside the common genital
opening; in neither case does the penis
penetrate as far as the bursa copula-
trix. In a number of dorid nudibranchs,
the arrangement of ducts is such that
the sperm must pass through the bursa
copulatrix. Thus it seems that the re-
ceptaculum seminis and bursa copulatrix
may each receive sperm, and although
their functions are not absolutely uni-
form, and although their positions vary
somewhat, a comparison between these
structures in opisthobranchs and proso-
branchs shows that they agree fairly
well in histology, function and position.
Among the opisthobranchs with an un-
divided pallial gonoduct and also
possessing both of these structures, the
receptaculum seminis is proximal, and
the bursa copulatrix is near the common
genital opening. When, in the forms with
a pallial gonoduct which has a Single,
internal division (Anaspidea, Cylindro-
bulla), the receptaculum seminis is
somewhat displaced toward the genital
opening, it is clear that the division
of the duct makes this possible. In the
Acoela, the arrangement of the bursa
copulatrix andthe receptaculum seminis,
which is here considered primitive, is
supported by a good series of inter-
mediate forms (Figs. 3,4). It is pri-
marialy among such forms as Acteon,
aeolid nudibranchs, pyramidellids and
pteropods, in which only one organ which
contains exogenous sperm is present,
that the criterion of position does not
hold strictly true and only the function
and structure are available to identify
these parts; but in these forms, the
systems display a greater similarity to
other forms in which the conditions here
considered primitive are present than to
each other. Again, inthe Sacoglossa, the
position, function and form of the struc-
tures which contain exogenous sperm are
highly variable; yet there isa good series
of interconnecting forms (Cylindrobulla,
Berthelinia) which allows a derivation
from the typical conditions, and the
atypical sacoglossan reproductive sys-
tems display no particular similarities
to those of any other group of mollusks.
Thus, while some other interpretations
are possible on the basis of part of the
evidence, those givenhere are more con-
Sistent with the comparative anatomy of
the system throughout the group.
The terminology and homologies of the
secretory portions ofthe pallial gonoduct
have long been confused. In opistho-
branchs, these structures are usually
called the “albumen gland” and the
“mucous gland,” according to the parts
of the egg mass which they are thought
to lay down. However, as Pruvot-Fol
(1960) has pointed out, this classification
fails to account for all the parts of the
egg-mass. Because the establishment
of the homologies and functions of these
secretory structures is essential to any
application of them in a comparative
study, I have studied them throughout
the order, and compared them with their
possible equivalents in the prosobranchs.
It has been demonstrated experimentally
(e.g., Kawaguti & Yamasu, 1961) that the
secretory structures form layers of
material around the eggs. The egg
masses formed by this process show
many features in common, differing
mostly in their proportions, and the
parts are readily comparable. Several
PHYLOGENY OF OPISTHOBRANCHS 335
studies have been published which relate
particular layers to the structures which
produce them. Further, the egg masses
have a structure such that the layers
must be laid down in sequence, and the
order of the secretory areas suggests
their probable functions. The secretory
areas in different groups show similari-
ties in histology and staining reaction
which likewise suggest homologies.
However, some variations in staining
reaction, and the absence of one of the
layers in many forms makes the estab-
lishment of homologies difficult. There-
fore, additional studies, aimed at com-
paring the detailed structure of the layers
and relating these layers to specific
secretory areas have been carried out.
The egg masses of opisthobranchs con-
sist, essentially, of eggs surrounded by
3 layers of protective and nutritive
materials. Comparable layers exist in
those of pulmonates and prosobranchs.
These layers willbe called, from interior
to exterior, the “albumen”, the
membrane, and the mucus. The “al-
bumen” has a nutritive function (Fretter
& Graham, 1962), and consists largely
of galactogen, sometimes mixed with
protein (Grainger & Shillitoe, 1952;
Horstmann, 1959). Around the “albumen”
is a thin layer whichI call the membrane;
this corresponds to the “coque
intérieure” of Pelsencer (1914), and to
the “egg covering” of Fretter & Graham
(1962). Outside of the membrane is a
layer or series of layers of a substance
called mucus. These layers will be
spoken of collectively as nidamental
layers, and the glands which secrete
them as nidamental glands.
Variations on this basic structure are
numerous, although the opisthobranch
egg mass is usually very simple. Any of
the nidamental layers may be absent. The
number of eggs contained in each mem-
brane varies considerably. The mem-
brane may have 2 or more twisted por-
tions, the chalazae, having no function;
they result fortuitously from the manner
in which the membrane is formed. In
some pulmonates and prosobranchs, one
or more additional layers, the capsule,
may be formed around the mucus.
The most recent general review onthe
structure of gastropod egg masses may
be found in the treatise of Fretter &
Graham (1962), which refers to older
works. Gabe (1962) has reviewed the
histochemistry of the nidamental glands
in the Mesogastropoda and provided
evidence for the structural and functional
uniformity of these parts. Besides a
large number of scattered references to
the egg masses of various opistho-
branchs, the general structure is well
treated by Thorson (1946) andina series
of papers by Baba and Hamatani (e.g.:
Hamatani, 1962). The presence of a
membrane seems to be almost universal
among opisthobranchs (cf. Eliot, 1910).
Lloyd (1952) seems to have overlooked
the membrane. Bolot (1886) describes
how the mucus may be separated from
the membrane by acid hydrolysis, and
gives a fairly detailed description of
the egg mass. Trinchese (1884) gives a
detailed drawing of the egg mass of an
aeolid nudibranch, showing the mem-
brane and chalaza. Trinchese’s (1893)
observation that the egg masses of
aeolid nudibranchs lack an “albumen”
layer has been overlooked.
Owing to the confused condition of the
literature, and to the fact that different
staining methods have been used to com-
pare the nidamental glands in different
animals, it was found expedient to carry
out a series of histochemical tests and
staining reactions ona variety of opistho-
branch egg masses. The results of these
follow.
Dendrodoris (Doriopsila) albopunctata
(Cooper, 1863) gave the best general
results. The mucus portion stained
metachromatically with Azure A,
strongly with haematoxylin and muci-
haematin, weakly with AB, and weakly,
but positively with Hale’s test; the PAS
reaction was very weak, while the DMAB
and Millon’s tests for protein were
negative; HgBPB gave only weak, back-
ground staining. These results strongly
suggest that the mucus is made up of
a sulfated, acid mucopolysaccharid con-
taining little or no protein. The mem-
336 М. T. GHISELIN
brane stained orthochromatically with
Azure A, gave only weak, background
staining with mucihaematin and AB, and
stained less intensely with haematoxylin
than did the mucus; the PAS reaction
was very strong; Hale’s test was weak,
as was eosin Staining; the DMAB,
HgBPB and Millon’s reactions were all
positive. These results are consistent
with the interpretation that the membrane
consists either of a neutral mucopoly-
saccharide mixed with protein, or ofa
mucoprotein. The “albumen” stained
very weakly and orthochromatically with
Azure A, and gave only background
staining with mucihaematin, AB, Hale’s
test and haematoxylin; it was stained
strongly by eosin, and gave a strongly
positive reaction with PAS; DMAB and
Millon’s tests were negative, andHgBPB
gave a weak background stain. Thus the
“albumen” consists of a neutral carbo-
hydrate, very likely, as in pulmonates,
galactogen (cf. Grainger & Shilitoe,
1952).
Egg masses of Hermissenda crassi-
cornis (Eschscholtz, 1831) were tested
with haematoxylin, eosin, mucihaematin,
Azure A, AB, PAS, and DMAB. Although
an “albumen” layer is not present inthis
form, and although the material did not
stain readily, the results were roughly
comparable with those on Dendrodoris,
except that with Azure A some of the
mucus did not show metachromasia and
the membrane showed a weak meta-
chromasia.
Egg masses of Hermaeina smithi
Marcus, 1961, were tested with Azure
A, mucihaematin, AB, haematoxylin,
eosin, PAS, DMAB, and HgBPB. The
staining reactions were similar to those
with Dendrodoris, but some differences
were noted. Mucihaematin, haema-
toxylin, and AB allowed a less-pro-
nounced distinction between the mem-
brane and the mucus; this would agree
with the results of Gascoigne (1956),
who worked with histochemically non-
Specific stains, on other sacoglossans.
The “albumen” showed distinctly positive
reactions with DMAB and HgBPB and
had some affinity for haematoxylin; the
“albumen” evidently contains some pro-
tein. It would seem that the carbohydrate
of the membrane in Hermaeina, and «
probably in other Sacoglossa as well,
differs somewhat from that of Dendro-
doris, but since the PAS and protein
reactions are all positive, it appears that
the difference lies mainly in the degree
of sulfation of the carbohydrate in the
membrane, as is suggested by the fact
that in H. smithi the membrane shows
a weak metachromasia with Azure A.
Egg masses of Acteon punctocaelatus
(Carpenter, 1864) were tested with muci-
haematin, haematoxylin, eosin, PAS, AB,
Azure A, DMAB and HgBPB. A layer of
“albumen,” if present, was too dilute to
be detected. The mucus stained to
varying degrees in the different parts
of the egg mass with AB, mucihaematin
and haematoxylin; only the outermost
layer showed metachromasia with Azure
A. Texts on the mucus with PAS, DMAB
and HgBPB were negative. The mem-
brane showed positive reactions with
HgBPB, DMAB and PAS; it stained
weakly with AB, mucihaematin, eosin
and haematoxylin; weak metachromasia
with Azure A suggests, again, some
sulfation.
The above results demonstrate that a
basic chemical uniformity exists in the
egg mass, but there is enough variation
that the parts cannot easily be dis-
tinguished on the basis of histochemical
tests alone; older work based on histo-
chemically non-specific staining re-
actions must be viewed with scepticism.
The nidamental glands should be given
names corresponding to the layers which
they secrete. As is shown in Fig. 1,
these are the “albumen” gland (al), the
membrane gland (me), and the mucous
gland (mu). The quotation marks around
the term “albumen” are given to dis-
tinguish it from a similar term used
by different authors, and to avoid the
implication that the secretion is pro-
teinaceous. Theterm “membrane gland”
is new, this structure usually having been
confused with either the “albumen” gland
PHYLOGENY OF OPISTHOBRANCHS 337
or the mucous gland; it corresponds
to the “winding gland” of the Anaspidea
(Eales, 1921). The mucous glandis often
called the “shell gland” in works dealing
with pteropods. Several criteria allow
the identification of these parts. The
most reliable of these is the dissection
or sectioning of an animal killed in the
process of laying eggs. The staining
reactions noted above may also allow a
distinction, but their reliability varies.
In general, the “albumen” andmembrane
are secreted in smaller droplets than
the mucus. The relative position of the
glands may indicate their function,
since the parts of the egg mass must
be laid down successively. The structure
of the membrane is such that it must be
laid down at the point of secretion;
therefore the membrane gland must be
so constructed that the eggs can pass
through it.
In various opisthobranchs the eggs do
not traverse the cavity of the “albumen”
gland. Rather, a specialization has
occurred in the gland such that there is
an area where the “albumen” is secreted,
and another, outside the gland itself,
where it is deposited around the eggs.
Such a modification has been demon-
strated conclusively only in the
Anaspidea (Eales, 1921) and Sacoglossa
(e.g.: Kawaguti & Yamasu, 1961). Evi-
dently this change allows a more rapid
and efficient deposition of “albumen”
and may prevent misdirection of
materials into the gland.
Invariably, the membrane gland con-
sists of tissue containing gland cells
interspersed with ciliated cells. For
functional reasons it never has a
separation into secretory and depo-
sitional areas. The membrane is a thin
film, which must be laid down ina sheet,
and any movement over a distance would
simply wad it into a tangled mass. The
cilia are necessary in the area of the
gland cells to insure the precise move-
ments of the membrane substance and
eggs. The eggs are moved through the
membrane gland and covered with a
sheet of this material (Gascoigne, 1956;
McGowan & Pratt, 1954). This process
has been described by Linke (1933) for
Littorina, a prosobranch. I have also
observed it in live Hermissenda crassi-
cornis, an aeolid nudibranch, and, with
less success, in various dorid nudi-
branchs. In H. crassicornis the eggs
are moved in series through the folds,
and sheets of membrane are secreted
around the series of eggs. The whole
series of eggs, along with its coverings,
is rotated, so that the eggs, either in-
dividually or in groups, are surrounded
by a sheet of membrane material. The
eggs, with their coverings, continue to
be rotated, andare separated into packets
of one or more eggs. After the membrane
has been laid down, the eggs shrink,
giving rise to a space which may easily
be mistaken for “albumen.” The process
in other opisthobranchs appears to be
essentially the same, although the details
vary. A peice of twisted membrane
(chalaza) often marks the spot where
the packets were twisted apart. The
number of eggs in a single membrane
varies considerably within the group,
as does the presence or absence of
“albumen.”
On the basis of Lloyd’s (1952) study
of Philine and Scaphander, and of their
own work on Acteon, Fretter & Graham
(1954) have concluded that in these
forms the eggs do nottraverse the cavity
of the so-called albumen gland. Although
it is impossible to disprove this view
at present, I disagree on the foilowing
grouds:
1. Fretter & Graham fail to explain
the mechanism of formation of the mem-
brane.
2. Lloyd overlooked the membrane.
3. What Fretter & Graham regard as
tubules in the so-called albumen gland
of Acteon tornatilis, Johansson (1954)
has described as folds. My own obser-
vations on A. punctocaelatus bear out
Johansson’s interpretation.
4. The apparent absence of a layer of
“albumen” in egg masses of Acteon
punctocaelatus (see above) suggests that
what Fretter & Graham call the albumen
338 — М. Т. GHISELIN
gland may be а membrane gland.
5. The conclusion that the eggs do not
enter the gland is based solely on the
observation of ciliary currentsinanaes-
thetized animals which were not laying
eggs. One may question the validity of
these experiments on the basis of the
fact that ciliary actionis readily modified
by chemical and nervous activity
(Hillenius, 1960).
Fretter € Graham (1954) have
suggested that in Acteon tornatilis the
eggs, with their membranes, are forced
into a pre-existing mass of mucus by
ciliary action. In A. punctocaelatus my
sections of egg masses show that the
eggs are arranged in a Series inside a
long tube of mucus of distinctly laminar
structure. This long tube is arranged
in a coil inside another layer of mucus,
forming an egg mass identical to that
described by Fretter & Graham for A.
tornatilis, and clearly similar to the egg
masses of other cephalaspideans. The
orderly arrangement of eggs within the
egg mass and the laminar structure of
the mucus’ throughout the Opistho-
branchia make it clear that the mucus
is secreted in layers as the egg mass
is moved through the gland. This process
has been demonstrated by means of
sections in sacoglossans (e.g.: Kawaguti
& Yamasu, 1961). By means of dis-
sections on animals in the process of
laying eggs, I have been able to demon-
strate that the mucus is laid down in
layers in a dorid nudibranch, Anisodoris
nobilis (MacFarland, 1905), and in an
aeolid nudibranch, Hermissenda crassi-
cornis, (cf. Mazzarelli, 1891; Thomp-
son, 1961b).
In euthyneurous gastropods generally,
the male and female systems are, or
have been, united into a common system
with a single, undivided gonoduct. The
pallial gonoduct may become divided into
Separate ducts. For an undivided pallial
gonoduct the term monaulic is used. In
diaulic and triaulic systems, the pallial
gonoduct has been divided into 2 and 3
ducts, respectively. As the etymology
suggests (aúdós, a pipe), these terms
should not be used to denote the number
of genital openings. Some confusion of
terminology has arisen because the
division of the ducts may be only partial.
It seems reasonable to base these dis-
tinctions solely on whether or not the
endogenous sperm, the exogenous sperm,
and the eggs have separate ducts (Eliot,
1910), especially since the extent of
division varies considerably. For the
separated ducts, the terms vas deferens,
vaginal duct and oviduct will be used.
The diaulic condition is formed by the
separation of either a vas deferens or an
oviduct. Because of the importance of
the distinction between the 2 kinds of
diaulic systems, Iintroduce the following
terminology. Androdiaulic: having a
separate vas deferens and an otherwise
undivided gonoduct (Fig. 2A), asin Acteon
(Fig. 2B; Fretter & Graham, 1954).
Oödiaulic: having a separate oviduct
and an otherwise undivided pallial gono-
duct (Fig. 2C), as in Aplysia (Fig. 2D;
Eales, 1921).
A discussion of the synonymies of the
terms used to describe the reproductive
system has been given by Pruvot-Fol
(1960); see also subsequent sections.
THE FUNCTIONAL BASIS OF
EVOLUTIONARY CHANGE
It has been maintained (e.g.: Lloyd,
1952) that the hermaphroditic repro-
ductive system in opisthobranchs arose
from the superimposing ofa male repro-
ductive system on a female one. There
is no way to test this hypothesis directly.
However, it provides a simple, gradual,
adaptive transition between conditions
in prosobranchs and those in opistho-
branchs. Further, the system resulting
from such a union provides a consistent
starting point for the derivation of the
various reproductive systems which
exist in the different groups of opistho-
branchs. The sudden superimposing of
the male and female system would
produce a highly inefficient structure
in the sense that the various functions
of the gonoduct might interfere with
PHYLOGENY OF OPISTHOBRANCHS 339
va
pr
ae rs AS ve
a -ca pr
al
bc
A Aller ” ca
me
т ом
В
FIG. 2.
Diagrams showing major variations.
an example of an androdiaulic system (simplified); C, idealized oödiaulic system; D, Apylsia
as an example of an oödiaulic system (after Eales, 1921, but simplified).
A, idealized androdiaulic system; B, Acteon as
al, “albumen” gland;
membrane gland;
seminis;
am, ampulla; bc, bursa copulatrix; ca, copulatory apparatus; me,
mu, mucous gland; ni, nidamental glands; pr, prostate; rs, receptaculum
sg, seminal groove; va, vas deferens; arrows, direction of movement of the eggs.
each other so much as to make the
change to hermaphroditism adaptively
deleterious. It seems reasonable to
assume that the union took place
gradually, with intermediate stages in
which the animals were protandrous
hermaphrodites rather than simul-
taneous ones. The selective advantage
of hermaphroditism has been discussed
by Tomlinson (1963), who argues that
it allows a low population density.
A hermaphroditic reproductive
system, formed by the superimposing of
a male system upon a female one, is
diagrammed in Fig. 1C. Such a re-
productive system, from which those of
all opisthobranchs may be derived, has
a number of inefficient features, and in
terms of these features one may explain
the major modifications and evolutionary
trends which occur in opisthobranch
reproductive systems. A list of what
appear to be the most important ofthese
inefficient features follows.
1. Storage of endogenous sperm inthe
ampulla interferes with the passage of
eggs through the ampulla, and the move-
ment of eggs through the ampulla could
eject the sperm stored there.
2. Since the endogenous sperm, exo-
820” М. Т. GHISELIN
genous sperm, and eggs must all move
through the undivided gonoduct, guided
at most by ciliary currents and by
grooves, the various elements could
easily be misdirected. Similarly, sperm
may be lost during transfer along the
open, external seminal groove.
3. The transfer of sperm by ciliary
action is slow.
The simplest solution to all of these
inefficiencies is the formation of 3
closed, separate ducts, one for each of
the 3 major functions of the original,
undivided duct. A complete division
of the male tract from the female,
embracing the gonad, coelomic gonoduct
and pallial gonoduct, appears never to
have evolved, but the pallial gonoduct
has developed a complete separation
more than once. In addition, a number
of other adaptations provide at least
partial obviation of the various inef-
ficiencies. A discussion of these adap-
tations follows, along with a more de-
tailed treatment of division.
1. The following mechanisms may be
considered adaptations which have helped
to alleviate interference between sperm
and eggs in the ampulla.
a. Sequential hermaphroditism. This
may represent the original con-
dition. It would not be a solution
to the problem where simultaneous
hermaphroditism is advantageous,
although combined with the storage
of exogenous sperm it would allow
the organism to function as a simul-
taneous hermaphrodite.
b. Emptying the ampulla when the eggs
pass through. This mechanism has
been reported (Mazzarelli, 1891)
for Aplysia, and may have been an
adaptation allowing simultaneous
hermaphroditism, but it has the
obvious disadvantage of wasting
sperm. Perhaps such wastage of
sperm is partly compensated for by
digestion of spermatozoa in the
bursa copulatrix; Lemche (1956)
has suggested that absorption of
misdirected materials may be the
major function of the bursa copula-
trix, but little precise information
in available.
c. Formation of separate coelomic
ducts for eggs andsperm. Such
an adaptation has been reported in
a nudibranch by Agersborg (1923),
but Odhner (1936) disagrees. Al-
though the ampulla has occasionally
been said to be partly divided, there
is no major group of opisthobranchs
which is demonstrably charac-
terized by such division; therefore,
such divisions, whether or not they
really exist, are primarily of
theoretical interest, in that they
illustrate one of many possible
adaptations.
а. Bypassing of the ampulla by the
eggs. In certain sacoglossans
(Pelseneer, 1894) the ampulla is a
diverticulum of the coelomic gono-
duct rather than a swelling, andthe
eggs do not enter it.
e. Formation of a ciliated tract which
moves the eggs around the sperm,
This adaptation is known in effective
form in nudibranchs.
f. Formation of a sperm-storage
organ in the male part of the system.
This modification has been reported
from some pyramidellids and
cephalaspideans (see below).
2. The following mechanisms prevent
misdirection of the sperm and eggs in
the pallial gonoduct.
a. Division of the duct. The pallial
gonoduct is often divided into a
system of separate tubes through
which individual materials pass in
a single direction.
b. Shortening of open grooves and un-
divided ducts. In many forms,
such as the Philinidae, the pallial
gonoduct as a whole has shortened.
As a result of this shortening, the
genital products have a shorter
distance to travel in the undivided
gonoduct, and therefore there is a
decreased likelihood that the differ -
ent functions will interfere with one
another or that the products willbe
misdirected out of the grooves
3.
PHYLOGENY OF OPISTHOBRANCHS 341
which conduct them.
. Simplification. The inefficiencies
of a structure may be overcome by
its loss. The structures most
commonly lost in opisthobranch
reproductive systems are those the
function of which may be discharged
by another structure. For instance,
of the 3 nidamental layers it is the
“albumen” layer which is most often
absent; the disadvantages of aloss
of nutritive “albumen” could readily
be compensated for by an increase
in the amount of yolk. Since the
bursa copulatrix and receptaculum
seminis both may contain exoge-
nous sperm, they are functionally
equivalent to some degree, and often
one or the other of these parts is
absent. In those forms which lack
a receptaculum seminis (Acteon-
idae) the bursa copulatrix occupies
the position characteristic of the
receptaculum seminis (Fig. 2B),
while in those forms which lack a
bursa copulatrix (aeolid nudi-
branchs) the receptaculum seminis
often is located in the position
characteristic of the bursa copul-
atrix (Fig. 4). In some instances
the receptaculum seminis and the
bursa copulatrix appear to have
fused into a single organ.
The following mechanisms hasten
the transfer of sperm.
a.
b.
Shortening of grooves. The short-
ening of the pallial gonoduct in
such forms as the Philinidae has
the advantage that the sperm have
less distance to travel from the
ampulla to the copulatory appa-
ratus. This is particularly signi-
ficant where the transport is by
ciliary action rather than by
muscular movement.
Prostate. Prostatic cells seem to
have been present in the common
ancestor of the Opisthobranchia.
They were probably present in the
pallial gonoduct and functioned in
forming a unitary mass ofsperma-
tozoa which could effectively be
moved through the open grooves
by ciliary action. In androdiaulic
and triaulic forms the movement
of sperm is largely by muscular
action, but the function of con-
gealing the sperm into a more or
less unitary mass is retained by the
prostate.
c. A separate, closed ejaculatory duct
or vas deferens. Such a modi-
fication may be only partial, asin
Philine (Pruvot-Fol, 1930) and
Cylindrobulla (Marcus & Marcus,
1956b), or it may be complete from
the beginning of the pallial gono-
duct to the end of the penis, asin
androdiaulic and triaulic forms.
d. Storage of sperm in the copulatory
apparatus, This adaptation allows
rapid copulation, since the sperm
may be transported slowly to the
copulatory apparatus along the
seminal groove when the animal is
not copulating, and stored there,
allowing rapid copulation at a later
time.
e. Reciprocal copulation. Where
copulation is reciprocal it should,
theoretically, take place twice as
fast as where the animals alternate
in the male and female roles.
Reciprocal copulation seems to be
largely restricted to the triaulic
and androiaulic forms (cf. Pruvot-
Fol, 1960), since the presence of a
penis in the gonoduct of a monaulic
or oödiaulic form would obviously
interfere with the passage of sperm.
However, as anaspideans (which are
oddiaulic) copulate in chains or
reciprocally (Fischer, 1869; Mc-
Cauley, 1960), it seems that a
separate vas deferens is not abso-
lutely essential.
As may be seen from the above dis-
cussion, the ancestral form of the
opisthobranch reproductive system can
be modified in a variety of ways such
that its inherent inefficiencies no longer
exist, or at least such that the effects of
these inefficiencies are decreased. In-
dependent lines of descent tend to under-
342 M. T. GHISELIN
go different adaptations which overcome
the same inefficiency. A change from
one kind of adaptation to a particular
inefficiency to another is not likely, since
once the inefficiency has been overcome,
there should be no selection pressure to
produce such a change. For example,
a change from an androdiaulic to an
oödiaulic type of reproductive system
is not to be expected, since it would
have no particular advantage; on the
other hand, a change from a diaulic to
a triaulic arrangement would con-
stitute a functional improvement, and
would be expected. The existence of
partial or imperfect adaptations to a
particular selective influence does not
prohibit the use of such partial or
imperfect adaptations, but only causes a
greater element of uncertainty to enter
into the interpretation. Given an adequate
understanding of the manner in which
the reproductive system functions, it
becomes clear that certain sorts of
change are clearly deleterious, and may
be rejected. For instance, there is no
reason to expect a triaulic reproductive
system to revert to the monaulic con-
dition with all its inefficiencies.
With an understanding of the manner
in which the parts function, it may be
possible to infer from peculiarities of
the reproductive system some of the
conditions under which the earlier stages
of evolution took place. Some of the
features of the reproductive systems
which occur in the Sacoglossa, as, for
example, the short duct which bypasses
the membrane gland in Limapontia (Fig.
5E, *), are best explicable in terms of
a specific kind of historical accident
which took place in their phylogeny, and
cannot be understood unless the manner
of function of the parts is known. Like-
wise, the diversity of imperfect solutions
to the fundamental inefficiencies of the
ancestral reproductive system (such as
Simplifications and the shortening of
grooves), which result in asystem which
functions far less well than a triaulic
one, can only be understood in terms of
their derivation from such an ancestral
form.
In addition, certain changes which may
be considered irreversible are of some
value in ascertaining relationships. In
Spite of the fact that the loss of a part
is easily produced, it can serve as a
sign of possible relationship; loss is
also useful in that any phylogenetic
derivation which requires the loss and
reconstruction of a complex part may
be considered dubious. Further, the
loss in different groups of different
parts which show some overlap in
function, such as the bursa copulatrix
and receptaculum seminis, may be in-
terpreted as divergent adaptations to
the same selective influence, suggesting
that both of the parts were present in
the common ancestor of the 2 groups.
In such reasoning, the possibility of
convergence is, of course, always
present. It follows that it is best to
minimize the possibility of being led
astray by convergence by the selection
of characters for comparison which are
more complicated than simple loss of
parts as well as relatively irreversible;
if this is done, convergence is improbable
and detectable.
In the present work, an attempt is
made to reconstruct the sequence of
evolution of the reproductive system
throughout the group in such a manner
that the sequence of forms is consistent
with the structural and functional po-
tentialities of the system, and with the
lines of reasoning outlined above. The
possibility of convergence in particular
features is fully admitted. However,
once the more likely courses of evo-
lution are hypothesized, it becomes
possible to evaluate other lines of evi-
dence in an attempt to reconstruct a
phylogeny which is consistent with the
structure and function of the reproductive
system, with evolutionary theory, and
also with analogous conceptions of the
changes of other structures and systems.
Any such study as this can only give a
partial contribution to the problem at
hand, and the ultimate criterion of the
truth of its findings can only be the
PHYLOGENY OF OPISTHOBRANCHS 343
degree to which it allows useful general-
ization.
A RECONSTRUCTION OF THE
PHYLOGENY OF THE REPRODUCTIVE
SYSTEM
The Opisthobranchia and Pulmonata
are often united on the basis of simi-
larities in the nervous system and other
structures into a single subclass, the
Euthyneura. The structure of the re-
productive system fully bears out this
interpretation, as the reproductive
system of all the Euthyneura can be
derived from an ancestral form very
much like that suggested below for the
opisthobranchs. Indeed, it appears that
one of the few characteristics which
occur throughout the Euthyneura, but
never in the Prosobranchia, is the
peculiar spermatozoon, which has a
Spiral filament wrapped around the head
and mid-piece, giving it a pronounced
screw-like appearance (Franzen, 1955).
A detailed discussion ofthe reproductive
system in the Pulmonata will not be
given here. The somewhat aberrant
‘Pyramidellidae, which are often con-
sidered prosobranchs, are included be-
cause their reproductive system is
comparable to that of the more typical
opisthobranchs.
The Reproductive System of the
Common Ancestor of the
Opisthobranchia
The ancestral opisthobranch probably
had an hermaphroditic reproductive
system somewhat like that diagrammed
in Fig. 1C. The degree to which it
was protandrous cannot be established,
since subsequent forms have evidently
tended to evolve in the direction of
simultaneous hermaphroditism. Those
forms in which protandry is most pro-
nounced, the pteropods, may have
reverted to this condition because of
their small size, whichhas the advantage
in pelagic organisms of retarding
sinking. The common practice of
designating certain opisthobranchs as
protandrous hermaphrodites simply
because the male gametes begin to
mature before the female is misleading.
These so-called protandrous her-
maphrodites probably function as simul-
taneous hermaphrodites since, by the
time they are able to function as males,
they are capable of storing exogenous
sperm in the viable condition until the
eggs ripen. It may be that the eggs
begin to ripen later simply because the
exogenous Sperm can be stored.
The pallial gonoduct included a re-
ceptaculum seminis, a bursa copulatrix,
and “albumen,” membrane and mucous
glands. In the primitive condition the
receptaculum seminis was situated at the
most interior part of the pallial gono-
duct and the bursa copulatrix near the
common genital opening. Such an
arrangement makes Zunctional sense,
since the receptaculum seminis should
have its duct in a position where the
Spermatozoa can be conducted to the
eggs before the latter receive their
coverings. It is a little more difficult
to justify the position of the bursa
copulatrix near the common genital
opening on purely functional grounds.
For dealing with waste materials, the
more distal position seems reasonable,
and the reception of the sperm mixed
with prostatic secretion by the bursa
copulatrix might most easily be ac-
complished by a bursa copulatrix having
a duct in a position where it can readily
receive the tip of the penis. But there
is no obvious reason why the spermato-
zoa Should not be deposited in the pallial
gonoduct near its opening and transferred
to a bursa copulatrix near the beginning
of the pallial gonoduct. The experi-
mental demonstration of Eales (1921)
that in Aplysia the sperm are deposited
in the pallial gonoduct suggests that
the deposition of the sperm in the bursa
copulatrix is not always necessary.
Perhaps the transfer of spermatozoa
through the pallial gonoduct is favored
by their prior removal from the prostatic
secretion. It may be that the distal
position is in part the result of ante-
344 M. T. GHISELIN
cedent historical conditions in which the
reception of the penis in the bursa
copulatrix was necessary. However this
may be, the position of the bursa copula-
trix near the common genital opening
is very commonin prosobranchs (Fretter
& Graham, 1962). In those opistho-
branchs with an elongate, undivided gono-
duct the bursa copulatrix is in this
same position, and where it is more in-
ternally located (Acteon, some sacoglos-
sans), the configuration of the system
is such that this condition can scarcely
be considered primitive. The variations
which occur within the group may be
explained in terms of the difficulty of
transferring sperm from the bursa copu-
latrix to the receptaculum seminis. In
all such deviant forms, there are one
or more special modifications, such as
those discussed in the preceding section,
which overcome the inefficiency of the
long, open duct with ciliated grooves,
which primitively connects these struc-
tures in mesogastropods and many
opisthobranchs. The argument must be
rejected that a condition in which the
bursa copulatrix and receptaculum semi-
nis are close together is primitive in
monaulic forms. The shortening of the
system as a whole provides a plausible
transition from conditions which occur in
mesogastropods, and has obvious func-
tional advantage in that it decreases the
distance which materials must traverse
in open grooves within the undivided
gonoduct, while the reverse change has
no such explanatory value. Polyphyle-
tic shortening of the pallial gonoduct
accompanied by an approximation of the
bursa copulatrix and receptaculum semi-
nis may be seen in such monaulic groups
as the family Aglajidae (cf. Guiart, 1901;
Marcus, 1955, 1961b; Pruvot-Fol, 1954;
Vayssiere, 1880; White, 1945, 1946).
The above lines of reasoning do not
necessarily conflict with Johansson’s
(1957) argument that the bursa copula-
trix of prosobranchs primitively occu-
pied a position near the beginning of the
pallial gonoduct, since he hypothesizes
different functional conditions among
early prosobranchs.
The nidamental glands were all folds
of tissue, composed of gland cells inter-
spersed with ciliated cells. The eggs
passed over the surfaces of these tis-
Sues, moved by the action of the cilia,
and the contents of the gland cells were
deposited over them. Such a condition
is known in certain Mesogastropoda
(Linke, 1933), and persists in such
opisthobranchs as the Doridacea
(McGowan & Pratt, 1954). It is diffi-
cult to establish which groups have been
modified by developing a condition in
which the eggs do not traverse the cavity
of the “albumen” gland, since this struc-
ture is often absent. If the nidamental
layers originated from the secretion of
gland cells in the ciliated epithelium of
the mantle, originally deposited as the
eggs passed over the epithelium, then
it would be more reasonable to assume
that the type of “albumen” gland which
is traversed by the eggs is primitive.
If one assumes that the condition in which
the eggs do not enter the gland is primi-
tive, one runs into difficulties in trying
to explain how such conditions were
evolved by natural selection. A change
from an arrangement in which the eggs
pass through the cavity of the gland to
one in which the area of secretion is
separated from the area of deposition
could easily be produced by a gradual
development of a tendency for the gland
to secrete into the nonglandular portion
of the gonoduct. The reverse change,
even if it should for some reason be
functionally advantageous, is less likely,
since unless the “albumen” gland were
completely and suddenly rearranged,
with not only a mechanism for moving
the eggs into the “albumen” gland and
out of it, but also for moving the eggs
across the secretory epithelium, the
change would have no adaptive signifi-
cance; in other words, the change can
go only one way without something like
a macromutation.
The mucous gland was primitively a
tube, perhaps folded to some degree.
A system in which the mucous gland
PHYLOGENY OF OPISTHOBRANCHS 345
has developed specialized secretory and
depositional areas is known only in the
Anaspidea (Mazzarelli, 1891); this condi-
tion may be the result of the large
size of the animal.
Probably a prostate was presentinthe
pallial gonoduct of the ancestral form.
Although the prostate tends to occupy a
position as part of the copulatory appa-
ratus, this was evidently not the original
location. The prostate is generally
pallial in the Prosobranchia (Fretter &
Graham, 1962); the Acteonidae include
members in which the prostate is closely
associated with the pallial gonoduct,
while in the closely related Hydatinidae
the prostate is part of the copulatory
apparatus; the prostate of the Pyrami-
dellidae is pallial. Evidently the pros-
tate facilitated the movement of sperm
in the open grooves.
The opening of the pallial gonoduct
was probably inside the mantle cavity,
as is the case with prosobranchs, and
with those opisthobranchs which retain
a more or less unmodified mantle cavity.
The penis was a projection on the side
of the head, and was connected to the
common genital opening by the open
seminal groove, which extended to the
tip of the penis. Sperm were con-
ducted along the groove by ciliary action.
Such an arrangement of the copulatory
apparatus is retained relatively unmodi-
fied in the Anaspidea (Eales, 1921), and
agrees well with that which occurs in
Mesogastropoda (Fretter & Graham,
1962). The position of the penis at a
distance from the common genital
opening was evidently a result of ances-
tral conditions in which the shell blocked
access to the pallial gonoduct. Probably
the penis was contractile, but lackeda
Sheath into which it could be withdrawn.
Some protection for the penis would
seem advantageous in burrowing gastro-
pods, and in most opisthobranchs this
protection takes the form of a penial
Sheath. In Acteon, as in some proso-
branchs, the shell gives protection to
the penis, and it seems reasonable to
infer that development of a sheath has
followed reduction of the shell. Sucha
Sheath could easily be evolved by in-
vagination of the body wall, and may
very well be polyphyletic.
Similarities in the Reproductive
Systems of the Acoela and the
Acteonidae and Related Forms
A number of similarities inthe repro-
ductive systems of the cephalaspidean
family Acteonidae and of the Acoela
(Notaspidea and Nudibranchia) suggest
that the groups may be related. The
evidence is rather tenuous, but the
possibility is real enough that it should
be considered in further research.
The reproductive system ofthe Acteo-
nidae shares with that of the Nudi-
branchia the possession of a particular
kind of ciliated strip in the ampulla
which moves the eggs around the sperm.
In Acteon, Fretter & Graham (1954)
describe a ciliated strip extending along
the wall of the ampulla; to each side of
this strip is a ridge of long cilia and
gland cells which evidently restrict the
eggs to the strip. I have sectioned the
ampulla of Triopha carpenteri (Stearns,
1873), a dorid nudibranch, and found
that the strip agrees very closely with
the description given by Fretter &
Graham of the ciliated strip in Acteon.
Thompson (196lb) notes the presence of
a ciliated strip in the ampulla of Tri-
tonia hombergi, a nudibranch of the sub-
order Dendronotacea, and describes how
the strip moves the eggs around the
sperm. Baudelot (1863) made a similar
observation on the movement of eggs
through the ampulla in Aeolidia papil-
losa, a nudibranch of the suborder Eoli-
diacea. I have observed transport of
eggs by the ciliated strip in Dendro-
doris albopunctata and in Hermissenda
crassicornis; in each case, the eggs
moved through the ampulla without be-
coming mixed with sperm. It should
be emphasized that more work on the
structure and function of the ampulla is
necessary, especially in smaller forms
such as Embletonia (cf. Chambers, 1934),
in which the ampulla seems to be some-
346 M. T. GHISELIN
what divergent in structure. In subse-
quent sections of this paper I show that
the ciliation in the ampulla of a variety
of opisthobranchs has been overlooked
or misinterpreted; furthermore the vari-
ation of the ciliated strip with physio-
logical condition, as described by Fretter
& Graham (1954), makes its interpre-
tation difficult. Be this as it may, the
ciliated strip shows some potential as
an indication of relationship since: (1)
it is fairly complex, (2) its adaptive
Significance is known, (3) there are
numerous other adaptations which can
and do produce the same effect of
getting the eggs past the sperm, and
(4) it seems not to vary much within
the Acoela.
A possibility exists that all the Acoela
and Acteonidae possess a pallial gono-
duct which is either androdiaulic or else
triaulic and hence derivable from the
androdiaulic condition. In so far as I
have been able to establish, there are
only 2 possible exceptions reported in
the literature, Rhodope (Marcus &
Marcus, 1952)and Umbraculum (Moquin-
Tandon, 1870). There is no reason for
considering Rhodope, which is minute
and aberrant, a member of the Acoela,
other than its concentrated nervous
system and lack of a shell. Riedl
(1960) has shown that the nervous sys-
tem of Rhodope is quite unlike that of
nudibranchs; he argues that the embry-
ology of the excretory system is closest
to that of the pulmonates. Umbraculum
should be reinvestigated by means of
serial sections; Eliot (1910: 91) states
clearly that Umbraculum has aninternal
vas deferens, although he gives no sup-
port for this statement. Similarly,
Pelseneer (1906) states that the Nota-
spidea are diaulic in the sense used
here.
The Reproductive Systems of the
Hydatinidae, Acteonidae and
Ringiculidae
The cephalaspidean families Acteoni-
dae (Bergh, 1901; Fretter & Graham,
1954; Johansson, 1954) and Hydatinidae
(Bergh, 1901) are characterized by a
closed vas deferens, and by having only
one structure containing exogenous
sperm (Fig. 2B). This sperm-containing
structure is located in the position
usually occupied by the receptaculum
seminis, but Johansson (1954) has shown
it to be a bursa copulatrix. Complete
separation of the vas deferens from the
pallial gonoduct in Hydatina has not been
demonstrated conclusively, but it seems
reasonable in the light of Bergh’s illus-
trations. The prostate in Acteon (Fretter
& Graham, 1954; Johansson, 1954) is
surrounded by the mucous gland, and
it appears that the only conspicuous
difference between the reproductive sys-
tems of the Acteonidae and of the Hyda-
tinidae is that in the latter family the
prostate has been displaced to the base
of the penis.
In Ringicula, whichis generally thought
to be related to the Acteonidae, Fretter
(1960) found that both bursa copulatrix
and receptaculum seminis are present
in the usual position, but was unable
either to find the vas deferens noted by
Pelseneer (1925) or to locate an exter-
nal seminal groove. In view of these
uncertainties, it is difficult to establish
the systematic position of the Ringicu-
lidae on the basis of the reproductive
system.
Reproductive Systems of the Notaspidea
From an ancestral form such as that
shown in Fig. 3A, I should derive all the
reproductive systems which may be found
in the Notaspidea and other Acoela, with
the possible exception of Umbraculum.
The evolutionary trends which occur in
the nudibranch reproductive systems
may also be seen in the Notaspidea.
The configuration shown in Fig. 3A is,
as discussed above, ineffecient in lacking
a separation between the nidamental
glands and the channel along which sperm
is transported from the bursa copulatrix
to the receptaculum seminis. The most
effective adaptation which would over-
come this inefficiency is the triaulic
condition (Fig. 3B), which occurs in
PHYLOGENY OF OPISTHOBRANCHS 347
va
bc
rs
Va bc
ya
wa bc
ni
Se a
va bc
er
FIG. 3. Diagrams showing variations in the arrangement of parts in the Notaspidea. Config-
urations shownare known from at least some members of the following taxa (see text); A, hypo-
thetical ancestor; B, Berthella; C, Pleurobranchaea; D, Berthelinia E, “Bourvieria” (sensu
Vayssiere).
am, ampulla; bc, bursa copulatrix; ni, nidamental glands; rs, receptaculum seminis; va,
vas deferens.
348 M. T. GHISELIN
such notaspideans as Berthella (Marcus
€ Marcus, 1955a) and in almost all dorid
nudibranchs. Most pleurobranchs, how-
ever, seem to have evolved different,
and less effective solutions. Isolation
of the nidamental glands, as occurs in
Pleurobranchaea (cf. Bergh, 1897-98),
prevents misdirection of sperm into the
nidamental glands (Fig. 3C). Subsequent
approximation ofthe receptaculum semi-
nis and bursa copulatrix (Fig. 3D) makes
two-way transport of materials in the
gonoduct unnecessary; such a configura-
tion is known in Berthelinia (cf. Lacaze-
Duthiers, 1859).
According to Marcus & Marcus (1959),
Pleurobranchaea hamva has a configu-
ration of the oviduct essentially like
that shown in Fig. 3A, except that the
bursa copulatrix has been lost. Absence
of the bursa copulatrix seems to be a
universal characteristic of the aeolid
nudibranchs, in which the receptaculum
seminis tends to occupy a position near
the mouth of the oviduct, and a variety
of pleurobranchs (Vayssiére, 1898, 1901)
seem to manifest this same tendency
toward a more external location of the
receptaculum seminis. A configuration
(Fig. 3E) has been reported in certain
notaspideans, e.g., in what Vayssiere
(1898) calls “Bouvieria ocellata”, in
which it appears that the spermatozoa
must be passed up the undivided ovi-
duct while the eggs are being laid; it
would seem that the movement of the
receptaculum seminis to the mouth ofthe
oviduct results in a functional disadvan-
tage. Yet most, if not all, work on the
reproductive system of notaspideans in
question deals primarily with superficial
configuration, and not enough is known
of function and internal structure to
exclude the possibility that the nidamen-
tal glands are actually quite isolated, as
in Fig. 3D. A possible explanation for
the movement of the receptaculum semi-
nis to the exterior in both notaspideans
and aeolid nudibranchs is a shift in
function as a result of which the sperm
are deposited in the oviduct, or evenin
the duct of the receptaculum seminis,
rather than in the duct of the bursa
copulatrix. There is evidence that such
a functional shift has taken place in
Pleurobranchaea meckeli (cf. Bergh,
1897-98). The result of such a shift
in function would be that a movement of
the receptaculum seminis towardthe ex-
terior would allowa more effective depo-
sition of sperm. One might object that
the position of the receptaculum seminis
at the mouth of the oviduct is primi-
tive; but this assumption does not ex-
plain such configurations as that shownin
Fig. 3C, and it provides a less satis-
factory transition from conditions which
occur in other groups.
Reproductive Systems of Dorid
Nudibranchs
The anatomy, histology and function
of the reproductive system in dorid nudi-
branchs have been exhaustively des-
cribed by Baudelot (1863), Bolot (1886),
Pohl (1905), Eliot (1910), Behrentz
(1931), Lloyd (1952) and McGowan &
Pratt (1954). The taxonomic literature
includes descriptions ofthe arrangement
of parts in large numbers of species.
In so far as reliable information is avail-
able, it appears that the reproductive
system of all dorid nudibranchs except
Bathydoris is triaulic. In contrast to
the aeolid nudibranchs, a bursa copu-
latrix is almost always present, and the
existence of an “albumen” gland has
been demonstrated (McGowan & Pratt,
1954).
Bathydoris appears to be the only di-
aulic dorid nudibranch (Evans, 1914).
Odhner (1934) has described a repro-
ductive system from Cadlina affinis
which, superficially at least, appears to
be diaulic, but the internal structure
seems not to have been studied. C.
affinis is one of many dorid nudibranchs
which are thought to have an imperfect
separation of the vaginal tract from the
oviducal tract. Odhner (1926) has sug-
gested that the degree of separation of
the 2 tracts may have systematic signi-
ficance, and postulates a series of
changes with the receptaculum seminis
PHYLOGENY OF OPISTHOBRANCHS 349
and bursa copulatrix both initially
opening near the vaginal orifice, a de-
velopment of a Separate vaginal duct,
and the gradual extension of the division
toward the coelomic gonoduct. However,
this sequence may be based largely on
superficial appearances. For instance,
MacFarland (1909) demonstrated that in
Discodoris voniheringi the vaginal and
oviducal tracts, which externally appear
only partly separated, are completely
separate within the glandular mass.
Odhner (1926) has discussed the func-
tional basis of some evolutionary trends
which he has observed in the mutual re-
lationships between the receptaculum
seminis and the bursa copulatrix. How-
ever, these trends are polyphyletic and
unidirectional, not showing any obvious
divergences, and therefore cannot serve
as a basis for the establishment of
clades. Unlike the reproductive system
in, say, sacoglossans or aeolid nudi-
branchs, that of the dorid nudibranchs
has not been shown to vary greatly
in the division of ducts or the manner of
function of the parts; such differences
form the basis of comparison inthe pre-
sent work. The differences within the
Doridacea are mostly a matter of pro-
portions of the parts and other minor
variations such as occur quite generally
in complex reproductive systems, but
which apparently have insufficient adap-
tive significance to allow their arrange-
ment in divergent series of adaptive
modifications. This lack of variation
within the Doridacea is perhaps the best
support for the functional arguments used
in the present study, since no evolu-
tionary change is expected where no
functional cause exists for it. I refer
the reader to the work of Pruvot-Fol
(1960) for a further discussion of some
variations of the reproductive system in
dorid nudibranchs.
The Reproductive System in Aeolid
Nudibranchs
The term “aeolid nudibranch” will, in
conformity with common usage, be
applied in the present discussion as a
collective term for organisms belonging
to the suborders Dendronotacea, Armin-
acea, and Aeolidiaceaof Odhner (1939).
The anatomy and histology of the repro-
ductive system in these forms have been
described in detail by Chambers (1934),
Lloyd (1952), and Thompson (1961b),
and further material is available in the
taxonomic literature. Before beginning
a discussion of the range of variation
and evolutionary history of the repro-
ductive system within the group, I will
comment on some uncertainties, contra-
dictions and misconceptions which exist
in the literature.
A prostate is occasionally said to be
absent (Odhner, 1939: 42); however, the
prostatic cells are usually, ifnotalways,
present (Thompson, 1961b), although the
prostate sometimes cannot be seen ex-
ternally. Similarly, Odhner’s (1936:
1068-1071) series of stages of the sepa-
ration of the male and female parts of
the pallial gonoduct of the Dendro-
notacea, including one in whichthe pros-
tate is not separate from the female
glands, reflects superficial appearances
only (MacFarland, 1923; Marcus, 1961b;
Thompson, 1961b).
If attachment of spermatozoa to the
wall of an organ which contains exogenous
spermatozoa is sufficient evidence ofits
homology to the receptaculum seminis
of other opisthobranchs, then no sound
evidence exists that any aeolid nudi-
branch has a bursa copulatrix. Odhner
(1939) states that the aeolid nudibranchs
have only one “vesicula seminalis.”
Attachment of spermatozoa in this struc-
ture has been reported by Trinchese
(1884) and various other workers.
Whether the receptaculum seminis was
located primitively near the opening of
the oviduct to the exterior (external
position, Fig. 4B), or in a more interior
position (internal position, Fig. 4A) has
been subject to inconclusive discussion.
Odhner (1939) suggests that the “bursa”
(i.e. the receptaculum seminis) hasbeen
displaced to the interior in some aeolid
nudibranchs, and points outthatthe posi-
tion of this organ may vary within a
350 M. T. GHISELIN
к
ni
am——
B
ni
Va
Any ie rs
ae
D
FIG. 4. Diagrams showing variations in the arrangement of parts in aeolid nudibranchs. Con-
figurations shown are known from at least some members of the following taxa (see text): A,
Hancockia californica; В, Tritonia (and numerous other forms); С, Doto; D, Armina.
am, ampulla; fc, fertilization chamber;
va, vas deferens.
single genus (Odhner, 1936: 1068). Func-
tional considerations make it seem more
likely that the receptaculum seminis was
internal in the common ancestor of the
aeolid nudibranchs; comparison with
other groups of opisthobranchs likewise
makes this seem reasonable. The ten-
dency for the receptaculum seminis to
become external in position is probably
polyphyletic, and this change is compen-
sated for by a variety of mechanisms
which allow the change. MacFarland
(1923) found that in Hancockia califor-
nica, a member of the Dendronotacea,
the receptaculum seminis is in-
ternal, and the nidamental glands are
only partially isolated from the rest of
the oviduct (Fig. 4A). According to
ni, nidamental glands; rs, receptaculum seminis;
Odhner (1936), the receptaculum seminis
in other species is external, and the
nidamental glands are more isolated
(Fig. 4B). H. californica represents
the ancestral condition if one reasons that
the nidamental glands have become iso-
lated because sperm tended to be mis-
directed into them in the ancestral condi-
tion, and that the receptaculum seminis
migrated to the exterior because sperm
were more easily deposited init andtwo-
way transport of materials in the un-
divided gonoduct became unnecessary in
the modified form. The reverse trans-
formation would have no adaptive basis,
unless one assumes that the nidamental
glands were completely unisolated from
the oviduct; in this case we should have
PHYLOGENY OF OPISTHOBRANCHS 351
to account for the original migration of
the receptaculum seminis to the mouth
of the oviduct. Such an alternative
interpretation, while possible, does not
explain such configurations as occur in
some species of Doto (Fig. 4C; cf.
Marcus, 1961b). Thearrangement shown
in Fig. 4B also occurs in Tritonia
(Thompson, 1961b), and its derivation
from a form in which the receptaculum
seminis occupied a more internal posi-
tion is strongly supported by embryo-
logical evidence (Thompson, 1962). The
conditions which are found in some
species of Doto (Marcus, 1961b) may
be considered an intermediate stage
(Fig. 4С). Odhner’s (1936) embryo-
logical evidence suggests that the tri-
aulic condition was evolved after the
receptaculum seminis in Dendronotus
became external, but tells us nothing
about the original conditions in aeolid
nudibranchs. In certain species of Ar-
mina (Marcus & Marcus, 1960b) the
nidamental glands remain opentothe rest
of the oviduct, the receptaculum seminis
is external, and a fertilization chamber
has developed in the position usually
occupied by the receptaculum seminis
(Fig. 4D). Apparently, the transfer of
sperm to the fertilization chamber
occurs prior to the descent of the eggs.
An analogous fertilization chamber
exists in such Aeolidiacea as Coryphel-
lina (Marcus, 1961a). Evans (1922) des-
cribes a fold in the oviduct of Calma
which allows the spermatozoa to pass
up the oviduct to the point of fertili-
zation while the eggspassthrough. These
varied modifications may easily be
understood as different adaptations to the
loss of the bursa copulatrix; they allow
the receptaculum seminis tobe external.
The internal position of the receptacu-
lum seminis in a number of aeolid nudi-
branchs bears out this interpretation,
if we assume that these forms have
happened not to develop a new mechan-
nism for getting the eggs past the sperm
to the point of fertilization while the eggs
are being laid.
The triaulic condition shows some pro-
mise as indicative of relationships, since
it would seem unlikely that such a con-
dition, once gained, would be lost. How-
ever, it is clear that the triaulic con-
dition has arisen polyphyletically, at
least once in the Dendronotacea and in
the Arminacea, and at least twice in the
Aeolidiacea. Some possible phylogenetic
inferences are suggested ina subsequent
section on the basis of attempts to group
triaulic forms together; however, these
are most uncertain not only because of
polyphyletic origin, but also because the
triaulic condition can easily be over-
looked. The following is a list of the
forms which have been reported in the
literature to be triaulic.
Dendronotacea
Dendronotus frondosus (Odhner,
1936)
Arminacea
Antiopella muloc (Marcus, 1958)
Janolus comis (Marcus, 1958)
Aeolidiacea
Pseudovermis spp. (Marcus &
Marcus, 1955b)
Miesea evelinae (Marcus, 1961a)
Embletonia fuscata (Chambers,
1934)
E. pallida (Marcus & Marcus, 1955b)
Dondice banyluensis (Portmann &
Sandmeier, 1960)
Aeolidia papillosa (Eliot, 1910)
Berghia coerulescens (Marcus,
1957)
Spurilla neapolitana (Marcus, 1957)
I have omitted Doto uva from the above
list, since the structure which Marcus
(1957) calls the fertilizing duct opens
near the mouth of the oviduct, and the
“vagina” opens into the penial sac; this
part is probably not a functional ferti-
lizing duct.
Reproductive Systems of the
Pyramidellidae
Almost all of our knowledge of the
reproductive system in pyramidellids is
due to the work of Fretter & Graham
(1949, 1962) and Fretter (1953). The
system is clearly monaulic, a sperm-
352 M. T. GHISELIN
containing organ is associated with the
copulatory apparatus, and the prostate
is pallial. In some pyramidellids the
seminal groove is not completely closed
to form a vas deferens or ejaculatory
duct (Fretter, 1953); it would appear
that a closure of the duct has arisen
within the group, since a closed duct
should be more effective in the trans-
ference of sperm. Although protandry
has been recorded, Fretter & Graham
(1949) have reported that sperm are pre-
sent in the ampulla when the eggs pass
through it; the mechanism which allows
the eggs to pass the sperm in the am-
pulla has not been discussed in the
literature. The presence of “albumen,”
membrane and mucous glands has been
demonstrated, and their functions deter-
mined (Fretter & Graham, 1949); these
glands are somewhat isolated from the
rest of the gonoduct, and communicate
with it by narrow ducts. Abursa copula-
trix is absent, and the receptaculum
seminis is quite distant from the common
genital opening; the ducts of the recep-
taculum seminis and of the various
nidamental glands are located quite close
together (Fretter & Graham, 1949). Such
a system could readily be derived from
the ancestral type suggested’ above for
the opisthobranchs; but the specializa-
tions of the copulatory apparatus, the loss
of the bursa copulatrix, and the concen-
tration of the nidamental glands makes
this system difficult to compare with
that of any other opisthobranch except
in the most general way. Not enough
is known of the reproductive system with-
in the Pyramidellidae to infer much about
evolution within the group.
The Oddiaulic Type
This type is a variation of the ances-
tral form in which the nidamental glands
have, to a greater or less degree,
acquired a separate, closed channel by
a division of the pallial gonoduct (Fig.
2C, D). Such a system, or one which
may be derived from it, probably exists
in all the Anaspidea, Sacoglossa and
Cephalaspidea of the family Diaphanidae
which have been sufficiently well studied
to allow a decision on this matter. The
oödiaulic system appears to be restricted
to these groups, and the thesis is here
maintained that it is monophyletic. Pos-
sibly, some pteropods, if not all, are
also oddiaulic.
Odhner (1926) has reviewed the struc-
ture of the reproductive system in the
Diaphanidae, and compares it to that
of the Anaspidea, not only on the basis
of the lack of a prostate associated
with the penis, but also because of the
general arrangement of ducts and
grooves. If Odhner’s “Spivalkanal” is
homologous to the “winding gland” in
the anaspidean Aplysia (Eales, 1921),
then the reproductive system in both
groups is essentially that shown in Fig.
2D. However, a receptaculum seminis
is apparently absent in the Diaphanidae
which Odhner describes, andthe division
of the duct in Aplysza is more extensive
than that of the Diaphanidae. Differences
in the gross appearance of the repro-
ductive systems of the 2 groups are
easily explained by differences in size;
the proportions of the parts, the extent
of the division of the duct and the way
in which the system is contracted into
a compact mass may vary to some
degree. That the “winding gland” of
anaspideans is the usual membrane gland
is clear from its position (Eales, 1921),
and also from its histology (Mazzarelli,
1891), the “winding gland” being the
only nidamental gland which has an
arrangement of secretory cells inter-
spersed with ciliated cells such that it
can secrete a membrane as the eggs
pass through it. There is also a good
agreement in the folded appearance and
in staining reaction (Inigier, 1907;
Odhner, 1926). Guiart (1901) states that
the winding gland forms the membrane
in the Anaspidea.
Evidence that the Sacoglossa were
primitively oödiaulic is somewhat more
tenuous, but Cylindrobulla, which is ap-
parently oödiaulic (Marcus & Marcus,
1956b), forms a good transition between
the Diaphanidae and such triaulic Saco-
PHYLOGENY OF OPISTHOBRANCHS 353
glossa as Berthelinia (Kawaguti €
Yamasu, 1961). Certain Sacoglossa are
said to be androdiaulic. However, a
critical review of the literature, dis-
cussed in detail below, has convinced
me that such views are either unfounded
or erroneous, or else are based on the
study of forms in which the diaulic
condition is clearly secondary. Inevery
study of the reproductive system in
sacoglossans which has involved a study
of serial sections of animals killed in
the process of laying eggs (Lloyd, 1952;
Gascoigne, 1956; Kawaguti € Yamasu,
1961), the animals studied were found to
be triaulic. The study of the repro-
ductive system in the Sacoglossa is ex-
ceedingly difficult, especially since the
function of the parts has only been re-
cently worked out. The parts are highly
complicated, and the division of the ducts
may extend over only a very short dis-
tance (Brüel, 1904) As Pelseneer
(1894) has pointed out, the division of
the ducts may occur very late in ontogeny.
Thus the theory that the Sacoglossa were
primitively oödiaulic remains somewhat
speculative, but there appears to be some
evidence for it.
The Anaspidea and Sacoglossa, in so
far as it is known, show a further
point of resemblance in having an “al-
bumen” gland of the type in which the
eggs do not enter the cavity of the gland.
No information is available on this
point for the Diaphanidae. In Aplysia
(Eales, 1921) the “albumen” is applied
in a fertilization chamber, and an “al-
bumen pouch” having this function has
been described for Berthelinia, a saco-
glossan (Kawaguti & Yamasu, 1961).
The fact that the bursa copulatrix
serves mostly as an organ which deals
with dead spermatozoa and other waste
materials, and not in receiving the
exogenous spermatozoa was demon-
strated experimentally for Aplysia by
Eales (1921); evidently, the duct of the
receptaculum seminis receives the exo-
genous sperm. The location ofthe bursa
copulatrix in some of the more modi-
fied sacoglossans at a point where it
cannot receive sperm directly at copu-
lation (cf. Gascoigne, 1956) suggests a
similar function throughout the oödiaulic
forms and those derived from them; it
may explain the proximity of the recep-
taculum seminis to the bursa copulatrix
in Cylindrobulla (Marcus & Marcus,
1956b) and other shelled sacoglossans.
The mechanism by means of which
the eggs were moved past the sperm
in the ampullae of the common ances-
tors of the Anaspidea and Sacoglossa
is difficult to determine. Nothing is
known about the histology or functional
anatomy of the ampulla in the Diaphan-
idae. In Aplysia, Mazzarelli (1891)
notes the presence of cilia in the am-
pulla, and observes that the eggs pass
through the ampulla and force a quantity
of sperm through with them. Eales
(1921) states that cilia are not pre-
sent in the ampulla of Aplysia, but
Marcus & Marcus (1957) do report the
presence of cilia in the ampulla, as
does Hirase (1929) for Dolabella. Becker
(1960) found that in the sacoglossan
Bosellia mimetica the eggs are able to
pass by the sperm in the ampulla.
Kawaguti & Yamasu (1961) say that
when the eggs pass through the ampulla
of Berthelinia, the bivalved sacoglossan,
they carry endogenous sperm with them.
In various species of Elysia (Pelseneer,
1894; Marcus, 1955) the ampulla is a
separate, blind pouch through which the
eggs do not pass. Ihave sectioned the
ampulla of Hermaeina smithi, and have
found that it contains a ciliated strip
in the form of a single, irregular ridge
of ciliated cells; it is quite unlike the
strip which occurs in Acteon or in the
Acoela. In addition to the ciliated
strip, the ampulla of H. smithi con-
tains numerous, tall secretory cells;
gland cells are said to be absent in the
ampulla of Limapontia and Alderia
(Lloyd, 1952). ,
From the above it seems, in so far
as information is available, that in both
the Anaspidea and Sacoglossa the ampulla
is far more variable than in the Acoela,
suggesting that adaptation to the problem
354 M. T. GHISELIN
of getting eggs past the sperm has taken
place within both the Anaspidea and Saco-
glossa. Direct observational evidence
is available to show that, at least in
some forms, this adaptation is only par-
tial. The homologies of the various
ciliated strips are hard to assess, but it
is possible that the common ancestor of
the opisthobranchs had some kind of
ciliated strip in the ampulla. However,
the available evidence suggests that the
ciliated strip is fully effective only in
the Acoela and perhaps the Acteonidae.
Evolution within the Sacoglossa
The only sacoglossan which does not
have avas deferens completely separated
from the pallial gonoduct is Cylindro-
bulla (Marcus & Marcus, 1956b), which
retains a large number. of primitive
features. Caliphylla (Brüel, 1904) is
said to have a short division of the
oviduct (Fig. 5A). In Berthelinia
(Kawaguti & Yamasu, 1961) this split is
far more extensive (Fig. 5B). In Lima-
pontia, Gascoigne (1956) and Lloyd (1952)
have described an arrangement which on
superficial examination looks very dif-
ferent from that of other sacoglossans
(Fig. 5E). In thiskindofsystemthe eggs
pass out of the coelomic gonoduct into
the pallial oviduct and pass to one end
of the membrane gland (Fig. 5E, *). In-
stead of entering the membrane gland,
however, they pass into a peculiar loop
(1) which conveys them to the other end
of the membrane gland, where they are
fertilized by spermatozoa from a kind of
modified receptaculum seminis (rs+),
and receive the “albumen” from the
“albumen” gland (al). They are then
covered by a membrane and pass to the
mucous gland (mu) where the egg mass
is completed. This configuration can
hardly be considered an effective mech-
anism for producing masses of fertilized
eggs, for one would think that a simple
triaulic system would function much
better. Probably the unusual configura-
tion is a result of historical accident.
Figures 5C and 5D show hypothetical
intermediate steps by which the condi-
tions in Limapontia (Fig. 5E) could be
derived from an arrangement similar to
that of Caliphylla (Fig. 5A). In Fig. 5C
a second split has developed in the ovi-
duct; such a split is known in various
sacoglossans. In Fig. 5D, the vaginal
duct (vd) has shortened, and the recep-
taculum seminis has fused with another
vaginal duct to form a complex struc-
ture (rs+). To allow a transition from
the configuration shown in Fig. 5D to
that shown in Fig. 5E, all that would be
necessary would be an extension of the
second split to the area of the duct of
the albumen gland. The somewhat un-
usual position of the bursa copulatrix
becomes readily understandable when it
is realized that in these forms this organ
has ceased to receive sperm at copula-
tion and functions as a receptacle for
dead sperm and other materials (Lloyd,
1952).
Lloyd (1952), on finding that Alderia
modesta has a reproductive system such
as is diagrammed in Fig. 5F, reasoned
that it was derived from a system like
that of Limapontia (Fig. 5E) by loss of
the bursa copulatrix and the communi-
cation between the undivided portion of
the oviduct and the membrane gland
(Fig. 5E, *). However, the arrange-
ment which exists in Alderia could just
as well have arisen by a modification
of a system with only one split in the
oviduct.
Some comments follow on the litera-
ture concerning reproduction in the saco-
glossans. The reproductive system of
these animals has been misinterpreted
largely because the membrane glandhas
been overlooked. Gascoigne (1956) and
Kawaguti & Yamasu (1961) have identi-
fied this structure. The staining reac-
tions of the membrane material are such
that the membrane gland is easily con-
fused with a part of the mucous gland;
the interpretations given here (Fig. 5)
are reinterpretations of older accounts
in the light of recent work on the mem-
brane gland. An attempt is here made
to group the sacoglossans according to
the number of splits in the oviduct and
PHYLOGENY OF OPISTHOBRANCHS 355
mu
va
am
€
vd
) Irs
al Me
va
bc
am
va
al
| | SEE
nay ==> PS+
GS de
mA
mu
F me mu
E
FIG. 5. Diagrams showing variations and hypothetical intermediate stages in the evolution ot
reproductive systems in the Sacoglossa. A, Caliphylla; B, Juliidae; C,D, hypothetical inter-
mediate stages; E, Limapontia; F, Alderia.
al, “albumen” gland; am, ampulla; be, bursa copulatrix; 1, loop; me, membrane gland;
mu, mucous gland; r, receptaculum seminis?; rs, receptaculum seminis; rs+, compound
structure including the receptaculum seminis; va, vas deferens; vd, vaginal duct. Arrows
show the path of the eggs; the asterisk indicates the short duct bypassing the membrane gland.
356 M. T. GHISELIN
the arrangement of the parts.
Berthelinia certainly has one splitand
only one (Kawaguti & Yamasu, 1961).
Pelseneer’s (1894) work on the shelled
Lobiger did not deal with the details of
internal structure of the pallial gono-
duct, and Marcus (1957) did not discuss
this question. According to Brüel (1904)
Caliphylla mediterranea has a small
internal division (Fig. 5A) which Marcus
(1958), who does not cite Brüel’s work,
may have overlooked. Gonor (1961)
gives a detailed description of a repro-
ductive system in Hermaeina in which
the division of the oviduct is single, and
Lloyd (1952) has described sucha system
in Alderia. Von Ihering (1892) demon-
strated that the reproductive system in
the shelled Oxynoe is triaulic, with a
well developed division, of the duct.
The doubly-divided oviduct certainly
exists in the Limapontiidae (Gascoigne,
1956; Lloyd, 1952; Pelseneer, 1894), and
in at least one species of Stiliger (Rao,
1937). It has also been described in
Elysia (Pelseneer, 1894; Marcus &
Marcus, 1959). Pelseneer (1894) des-
cribes a system in Elysia viridis in
which the oviduct is doubly-divided, and
in which the duct of the bursa copula-
trix also shows a division; this may be
considered a variation. Becker (1960)
illustrates a system of Bosellia in which
there appear to be 2 splits in the ovi-
duct, suggestive of conditions to be
found in Elysia. Among these forms,
the type of reproductive system which
occurs in the Limapontiidae has also
been found in Hermaea dendritica
(Pelseneer, 1894) and in Stiliger (Rao,
1937).
From the fact that, according to
Pelseneer (1894) the opening of the va-
ginal duct occurs late in ontogeny, or,
according to Gascoigne (1956), never at
all in some modified forms, I question
the view of Marcus (1955, 1958) that
Elysia is sometimes diaulic. Similarly
inconclusive are a number of interpre-
tations of Marcus (1957, 1958) and of
Marcus € Marcus (19564) of several
species of Stzliger in which the “albumen”
gland is depicted as entering the so-
called mucous gland at a point which
probably corresponds to the transition
between the division between the mem-
brane and mucous glands, because such
an arrangement would not function; how-
ever, they describe these animals as
triaulic, if somewhat different from the
form described by Rao (1937).
Marcus & Marcus (1960b) argue that
Tridachia crispata is diaulic, because
they found no separate vaginal opening.
But since they say that the female germ
cells were immature, since the entrance
of the “albumen” gland into the gonoduct
before the latter bifurcates may be taken
as a sign of immaturity, and since a
partial bifurcation, such as occurs in
Caliphylla may have been overlooked
or have been still unformed, their inter-
pretation is open to question.
Conditions in the genus Hermaea are
most uncertain. Pelseneer’s (1894)
account of Hermaea dendritica shows that
a system of the Limapontia type (Fig. 5E)
is present in at least some members of
the genus. Pelseneer (1894) states that
H. bifida is diaulic, and Marcus (1955)
likewise considers the oviduct of H,
coivala to be undivided. Again, a con-
nection may have been overlooked, es-
pecially since the membrane and mucous
glands have not been studied in detail.
Briiel (1904) argued that H. bifida does
not fit well into the genus Hermaea,
and if the genus is artificial, then the
deviant condition of the reproductive sys-
tem might well be explained. Derivation
of the Limapontia type of reproductive
system from that which occurs in the
allegedly diaulic Hermaea species seems
improbable; either the Limapontia type
would have to be biphyletic, which, owing
to the complexity of the system is un-
likely, or else the continuity which Ihave
shown between the various sacoglossan
reproductive systems is erroneous,
which is admittedly a possibility. If H.
bifida and H. coirala are actually diaulic,
the reproductive system is still some-
what atypical, and probably modified,
since the bursa copulatrix is quite in-
PHYLOGENY OF OPISTHOBRANCHS 357
ternal. It may be that this system has
arisen through a secondary simplifi-
cation of a Limapontia type of repro-
ductive system. Such a simplification
may be advantageous in a highly compli-
cated system, and would not constitute
an exception to the general rule that a
triaulic system does not revert to the
diaulic condition, since the Limapontia
type is doubly triaulic and probably de-
rived from one in which the triaulic
condition was only partial. Simplifi-
cation of function is known in the form
of hypodermic impregnation by way of the
haemocoel in Alderia (Hand & Steinberg,
1955), and analogous simplification may
explain many anomalies in the construc-
tion of the sacoglossan reproductive sys-
tem.
Further research on the anatomy of
sacoglossan reproductive systems is
necessary to clear up the uncertainties
mentioned above. My interpretations and
criticisms must be considered hypothe-
tical, especially in the light of the great
apparent variability of the system within
the group, which makes any comparative
interpretation highly speculative. Brüel
(1904) argued that the reproductive sys-
tem in the sacoglossans was primitively
triaulic, suggesting that the division of
the oviduct has become less extensive
secondarily. I am inclined to argue
that the reproductive system in sacoglos-
sans was primitively oddiaulic (as in
Cylindrobulla) and later became triaulic,
since this assumption allows a transition
from other groups of opisthobranchs to
such forms as Berthelinia which have
a system differing very little from the
usual opisthobranch arrangement; fur-
ther, it allows a consistent derivation of
the reproductive systems of those saco-
glossans in which the reproductive sys-
tem is best known. But polyphyletic
increase in the extent of the division
of the duct seems to me more reason-
able in terms of functional advantage.
Reproductive Systems of the
Acochlidiacea
The Acochlidiacea are, in general,
small, mesopsammal organisms, and
show various kinds of reduction which
obscure their relationships. Gonochor-
ism, loss of the penis, and formation
of spermatophores may be taken as
secondary simplifications resulting from
small size in the Microhedylidae (cf.
Kowalevsky, 1901; Marcus, 1953; Marcus
& Marcus, 1954), since other groups of
acochlidiaceans show a more typical
reproductive system, and reconvergence
is not likely. The reproductive system
of the Hedylopsidae has been treated by
Odhner (1937) who shows that the seminal
groove is open, although a closed ejacu-
latory duct associated with what he calls
a “vesicula seminalis” is present. The
copulatory apparatus in the Hedylopsidae
has also been described by Kiithe (1935);
the copulatory apparatus would appear,
at least superficially, to resemble that
of the Pyramidellidae, if Odhner’s term
for the appendage of the ejaculatory
duct actually corresponds toits function.
In so far as I have been able to tell
from published accounts, there is no
internal division of the pallial gonoduct
in the Microhedylidae or Hedylopsidae,
and it would appear that this condition
was primitive in the group, although
reduction due to small size cannot be
excluded. In view of Odhner’s (1937)
suggestion of a possible relationship be-
tween the Acochlidiacea and the Dia-
phanidae, further work should be di-
rected toward attempting to establish
whether or not such a division exists.
At present there is no good evidence
in the structure of the reproductive
system in the Acochlidiacea which sug-
gests an affinity to any other order of
opisthobranchs, beyond those features
clearly derived from the common an-
cestor of the Opisthobranchia.
A Comparison of the Reproductive
Systems of the Remaining
Cephalaspidea and of the Pteropods
All of the cephalaspideans not dis-
cussed so far (Scaphandridae, Philinidae,
Aglajidae, Gastropteridae, Bullidae,
Runcinidae, Atyidae, Retusidae and
358 — M. T. GHISELIN
Philinoglossidae) are monaulic, and re-
semble the pteropods in having a pros-
tate associated with the copulatory ap-
paratus. The degree to which this simi-
larity may be taken as an indication of
relationship cannot be determined at
present. The monaulic condition indi-
cates only that these animals are not
descended from diaulic forms; likewise
the prostate could easily have attained
its present position polyphyletically.
Nonetheless, a clear relationship does
seem to exist between many of these
forms, and they will be treated together
for convenience. As the pallial and
coelomic gonoducts do not seem to vary
greatly in these forms, the relation-
ships must be determined largely on the
basis of the copulatory apparatus.
Diagrams of a number. of copulatory
apparatuses are given in Fig. 6; among
these, the most primitive type would be
that which has an open seminal groove
extending to the tip of the penis, and a
prostate secreting into the seminal
groove (Fig. 6A). Such a copulatory
apparatus has been reported from the
Gymnosomata (Morton, 1958), and from
a variety of cephalaspideans. The funda-
mental inefficiency of this kind of copu-
latory apparatus lies in the transfer of
Sperm by open grooves during copulation;
Sperm would be expected to leak out of
the groove and to be moved only slowly
by ciliary action. The inefficiency of
Open grooves in general is especially
great in the copulatory apparatus; ob-
viously, when the penis is thrust into
the vagina, transfer along the open
groove on the penis is particularly dif-
ficult owing to mechanical deformation.
The most obvious improvement over the
primitive arrangement would be the
formation of a closed ejaculatory duct
(Fig. 6C, E); this modification seems
to have arisen separately within several
natural groups but is usually not ac-
companied by formation of a completely
closed vas deferens. This frequency of
only partial modification suggests that
the closure of the seminal groove in the
copulatory apparatus itself has particu-
larly great functional advantage. Other
modifications of the copulatory apparatus
can produce the effect of hastening the
transfer of sperm and preventing the
loss of sperm from open grooves. One
of these modifications (Fig. 6B) involves
the development of a sperm storage
organ (spermatic bulb) as a part of
the copulatory apparatus; sperm are
transferred to the copulatory apparatus
before copulation. These differing adap-
tations which overcome the same inef-
ficiency cannot readily be derived from
each other, and therefore can be looked
upon as divergences, hence as good
signs of lack of relationship; as indi-
cations of natural groups their useful-
ness is somewhat more limited, owing
to the relative simplicity of their struc-
ture and the probability of convergence.
Cephalaspideans with a Spermatic Bulb,
and Possibly-Related Forms
In a number of cephalaspideans the
copulatory apparatus is so modified that
it contains a sperm-storage organ, the
spermatic bulb (Fig. 6B). In at least
some of these forms the prostate
has taken on the function of pro-
ducing spermatophores. The duct of
the prostate functions as an ejacula-
tory duct. A penis may be present,
but usually the everted penial sac-serves
this function, especially in the smaller
forms. This kind of copulatory appa-
ratus occurs in the families Atyidae
(Marcus & Marcus, 1959), Bullidae
(Marcus, 1957), Runcinidae (Ghiselin,
1963), Philinoglossidae (Marcus, 1953),
and Retusidae (Marcus & Marcus, 1960b).
It also occurs in Tornatina (Marcus,
1956), which has been variously placed
in the Retusidae and Scaphandridae.
This type of copulatory apparatus ap-
pears to be somewhat variable in mor-
phology, especially in the form of the
prostate; hence its fundamental uni-
formity in physiology has tended to be
overlooked. Spermatophores have been
observed in Haminoea (Perrier €
Fischer, 1914), and in Runcina (Ghiselin,
1963). Marcus & Marcus (1960) say
PHYLOGENY OF OPISTHOBRANCHS 359
FIG. 6. Simplified diagrams showing the arrangement of parts in the copulatory apparatus of
certain cephalaspideans. A, ancestral form; B, Atyidae, etc.; C, Philine aperta; D, Philine
alba; E, Scaphander lignarius.
at, attachment of prostate to penial sac; dp, duct of prostate; ds, seminal duct; ed, ejacula-
tory duct; o, opening to seminal duct; op, opening of the prostate; pe, penis; pr, prostate; ps,
penial sac; sb, spermatic bulb; sg, seminal groove.
360
that Rhizorus may produce a spermato-
phore. Although Perrier & Fischer
(1914) searched in vain for spermato-
phores in Bulla, this negative evidence
is hardly conclusive, since in Runcina
spermatophores are only occasionally
present (Ghiselin, 1963).
This modified copulatory apparatus is
quite distinctive, in spite of its varia-
bility in some forms. The evidence
that it exists in all members of the
families and genera mentioned above
is, admittedly, somewhat ambiguous.
Odhner (1924) did not find a spermatic
bulb in Runcinella, but his animals may
have been immature. Burn (1963) states
that a spermatic bulb is absent in some
of the Runcinidae, but it is clear from
his drawings that the copulatory appara-
tus is very similar to that of other mem-
bers of the family in which a sper-
matic bulb is present. Marcus (1961b)
notes that a spermatic bulb is some-
times said to be absent in Bulla gould-
tana; Specimens which I have examined
vary in its development, suggesting that
the spermatic bulb is only present in ani-
mals which are in breeding condition. I
have not been able to obtain specimens of
В. gouldiana in which the presumed
spermatic bulb is well developed.
Sections of the copulatory apparatus in
which the presumed spermatic bulb was
quite small did not reveal the presence
of spermatozoa, although the lumen was
full of the usual eosinophilic, corpuscular
secretion. It appears that the tubular
structure mentioned by Marcus (1957,
1961b) is homologous to the prostate of
other cephalaspideans.
Reproductive Systems in the
Scaphandridae, Philinidae, Aglajidae
and Gastropteridae
As Pruvot-Fol (1954) observes, the
systematic interrelationships between
these families are very much in doubt.
The Scaphandridae would appear to be a
highly diverse group of forms which are
united mainly on the basis of their ex-
ternal shell and relatively unmodified
digestive system; these are primitive
M. T. GHISELIN
characteristics not likely to reveal re-
lationships. Some forms with a sperm-
atic bulb are often placed in the Scaphan-
idae, and it seems likely that anadaptive
radiation took place at a grade of evo-
lution attained by the more primitive
members of the family, leading toforms
with a spermatic bulb on the one hand,
and to a clade including Scaphander, the
Philinidae, the Aglajidae andthe Gastro-
pteridae on the other. The difficulty of
placing these forms in a systematic
arrangement results, if this postulated
adaptive radiation did occur, from
subsequent parallel and convergent
changes.
The clade which includes the Philinidae
is fairly generally recognized, although
its precise interrelationships remain
obscure (cf. Pruvot-Fol, 1954; Boettger,
1954). There appears to beatrend with-
in the group for a reduction of the shell
and radula. In Scaphander the shell is
external, and the radula formula is I-1-I;
in Philine and the Gastropteridae the
shell is internal, and the radula formula
is I-O-I or n-I-O-I-n; in the Aglajidae
the shell is internal and the radula is
absent; in certain Philinidae, all Aglaj-
idae and the Gastropteridae, the gizzard
plates have been reduced or lost (Pruvot-
Fol, 1954). Pruvot-Fol (1954) has
commented on the difficulties of deciding
whether certain exotic forms should be
placed in Scaphander or in Philine.
Such uncertainties and the general
tendency for a loss of the shell and of
the hard parts of the gut make it appear
likely that parallel developments have
taken place. A consideration of the
implications of the reproductive system
for the evolution of the group follows,
because of its theoretical interest and
because it clarifies some questions
raised in the literature (Pruvot-Fol,
1960). More definite conclusions as to
the relationships between the various
groups must await the accumulation of
additional evidence.
The coelomic gonoduct of certain
Scaphandridae and related forms has
a section in which there are numerous
POOP Sw
PHYLOGENY OF OPISTHOBRANCHS 361
secretory cells of unknown function.
The histology of this secretory area
has been described for Cylichna by
Lemche (1956), and for Philine and
Scaphander by Lloyd (1952). The
probable homologue of this structure may
be seen in Guiart’s (1901) diagrams of
the reproductive systems of Aglaja and
Gastropteron. The ampulla of Cylichna
has been reduced, evidently because of
the small size of this form (Lemche,
1956). In Philine alba my sections
show the presence of a ciliated band
which extends through the length of the
ampulla. A series of secretory cells
and long cilia, such as may be found
in Acteon and the nudibranchs, was not
observed, although the possibility that
the animal studied was not in breeding
condition cannot definitely be excluded.
In the Aglajidae, a closed ejaculatory
duct is sometimes present, but in a
number of forms the seminal groove
extends to the tip of the penis (Marcus,
1961b). A prostate is present, often in
the form of a pair of lobes. The
copulatory apparatus in this family has
not been studied in sufficient detail to
allow a detailed comparison with other
forms.
The copulatory apparatus of Philine
aperta (Fig. 6C) has been described by
Pruvot-Fol (1930) and studied in detail
by Lloyd (1952). The seminal groove
(sg) enters the penial sheath, where it
communicates with the opening (o) of a
sperm duct (ds). This sperm duct joins
with the duct of the prostate (dp) toform
a divided tube with a common muscular
sheath, but with a distinct partition be-
tween the 2 ducts. Inside the penis
(pe), the 2 separate ducts unite to form
a single ejaculatory duct (ed). The
prostate (pr) is a very long, closed tube
which is attached by a strand of tissue
to the penial sheath. According to
Pruvot-Fol (1960) this type of copulatory
apparatus probably exists in a number
of species of Philine, but not in all.
Lloyd (1952) has studied a somewhat
different copulatory apparatus in Scaph-
ander lignarius (Fig. 6E), in which the
seminal groove communicates with the
ejaculatory duct (ed) through a pore (о)
at the base of the penis. The prostate
(pr), in the form of a bulb with secretory
tubules, communicates with the ejacula-
tory duct (ed) via a short duct.
Mattox (1958) has described a copula-
tory apparatus in Philine alba which
resembles that of Scaphander lignarius
except that there is an open seminal
groove instead of a closed ejaculatory
duct (Fig. 6D). By means of serial
sections I have been able to verify and
Supplement Mattox’s observations. The
seminal groove (sg) enters the opening
of the duct of the prostate (dp). The
surface of the prostate is increased by
a folded projection of one of the walls,
not by tubules as in Scaphander. The
prostate and its duct are surrounded by
a layer of circular muscles, which
Suggests that the prostate functions as
an ejaculatory vesicle. The epithelium
of the prostate secretes the usual cor-
puscular, eosinophilic substance.
Lloyd (1952) suggests that the copula-
tory apparatus of Scaphander lignarius
(Fig. 6E) arose from one like that of
Philine aperta (Fig. 6C) by concentration
of the prostate and shortening of the
ducts. If this interpretation is correct,
and if the kind of copulatory apparatus
found in P. aperta is not polyphyletic,
then it follows that the genus Philine
has been derived from Scaphander at
least twice. Lloyd's suggestion would
demand a cladogenesis between P. aperta
and S. lignarius before the shell became
internal and the rachidian tooth was lost,
or else a complex reconvergence in a
direction opposite to the usual trend
with no functional advantage. Other
alternatives are possible, but in any
case, it is difficult to rationalize a
monophyletic origin of Philine with a
monophyletic origin of the ejaculatory
duct. In view of the imperfect present
state of knowledge, it would seem most
reasonable to assume that the repro-
ductive systems with ejaculatory ducts
are derived polyphyletically froma form
without an ejaculatory duct, since the
362 M. T. GHISELIN
details of structure in the copulatory
apparatus of the 3 forms described
above are only generally comparable.
Likewise the Aglajidae would appear
to have developed from forms in which
the seminal groove was open along the
penis, and do not show clear relation-
ships to any of those Scaphandridae or
Philinidae in which the copulatory
apparatus has been studied in detail.
About all that is known of the copula-
tory apparatus in the Gastropteridae
is that the prostate is elongate and
a closed ejaculatory duct is present
(Guiart, 1901). Hence, a derivation
of the copulatory apparatus of
the Gastropteridae from the kind of
copulatory apparatus which occurs in
Philine aperta cannot be excluded. But
if the conditions in P. aperta and the
Gastropteridae did arise monophy-
letically, then the Aglajidae and Gastro-
pteridae cannot be derived as a Single
clade from the Philinidae, as Boettger
(1954) suggests.
Reproductive Systems of Pteropods
Because of their relatively small size,
the animals placed in the orders of
pteropods, Gymnosomata and Theco-
somata, display a fairly simple struc-
ture in most features of their anatomy.
Both groups are so highly modified that
their relationships are most uncertain.
They have often been considered biphy-
letic (Pelseneer, 1888). The similari-
ties in the reproductive systems of the
2 groups make it expedient to treatthem
together, whether or not these simi-
larities reflect a monophyletic deriva-
tion.
Recent work of Morton (1954, 1958) on
the thecosomatous pteropod Spiratella
and on the gymnosomatous pteropod
Clione agrees fairly well with most older
work in suggesting that the reproduc-
tive system is monaulic. Yet in neither
of these works does Morton take issue
with the findings of Meisenheimer (1905)
who, in several systematically isolated
forms within each order, found a kind
of bifurcation in the pallial gonoduct,
which suggests that the system is
oödiaulic. This discrepancy could mean
that the oddiaulic condition has arisen
several times, or it could mean thata
connection has been overlooked. The
secretory structures are rather intri-
cately folded, and an inner connection
could easily be overlooked, especially
if its presence is not anticipated.
Minichev (1963) has specifically dis-
puted the view of Meisenheimer (1905)
that the pallial gonoduct of Hydromyles
globulosa, the most “primitive” gymno-
somatous pteropod, is divided into 2
tubes. Yet Minichev’s opinion is some-
what questionable, in view of the fact
that he only studied the male stage of
this protandrous, viviparous form.
Certain Thecosomata show, ifweac-
cept Meisenheimer’s (1905) interpreta-
tion, a close agreement with the Dia-
phanidae in the structure of the pallial
gonoduct. What Meisenheimer (1905)
and Morton (1954) call the albumen gland
is, from the staining reactions of Hsiao
(1939) and its position, a membrane
gland. An “albumen” gland is, at least
in some forms, absent, and the mem-
brane gland is drawn out into a spiral.
The “Schalendrüse” corresponds to the
mucous gland.
The histological details of the nida-
mental glands given by Meisenheimer
(1905) likewise allow an establishment
of homologies in some gymnosomatous
pteropods. In Pneumoderma what he
calls the albumen gland has a single
opening and was found to be full of
secretion; it thus shows, as is borne
out by its histology, a resemblance to
the “albumen” gland of anaspideans.
The “Schalendrüse” in both Clionopsis
and Pneumoderma includes 2 secretory
areas differing in the kind of secretion,
which, from their position and their
histology, correspond to the membrane
and mucous glands of other opistho-
branchs.
In both groups, only one sperm-con-
taining organ is associated with the
pallial gonoduct, but Pruvot-Fol (1954)
notes that in some forms it is bifurcated
PHYLOGENY OF OPISTHOBRANCHS 363
and suggests that it may be homologous
to both the bursa copulatrix and the
receptaculum seminis of other opistho-
branchs. In Spiratella, a thecosomatous
pteropod, Hsiao (1939) has described a
two-part “receptaculum seminis” in
which there are 2 kinds of epithelium;
in one part the spermatozoa were found
to be normal, and in the other they were
degenerating. The inference seems not
unreasonable that the reproductive sys-
tem in both these groups has been simpli-
fied by the union of the receptaculum
seminis with the bursa copulatrix. Whe-
ther this similarity is only superficial,
is due to convergence, or reflects
common ancestry is hard to judge;
certainly it is unusual.
The copulatory apparatus in both
groups includes a prostate such as may
be found in many Cephalaspidea but not
in Anaspidea. The seminal groove may
be partly closed off to form an ejacula-
tory duct in some members of both
groups, but in others it is open (Meisen-
heimer, 1905; Morton, 1954,1958). A
variety of complications and speciali-
zations of the copulatory apparatus are
known in both groups, but these have
no particular parallel in other opistho-
branchs (cf. Bonnevie, 1916; Tesch,
1950; Pruvot-Fol, 1960).
Until the above-mentioned conflict
in the literature is resolved, a com-
parison between the reproductive sys-
tems of pteropods and other opistho-
branchs must be highly speculative. Yet
it would appear that a fairly soundargu-
ment can be made for a monophyletic
derivation of the pteropod reproductive
system. Further, if an affinity between
the Gymnosomata and Anaspidea is main-
tained, a similar affinity should be sup-
ported for the Thecosomata.
PHYLOGENETIC INFERENCES
In the previous discussion an attempt
has been made to compare the repro-
ductive systems of the opisthobranchs
and to arrange them in probable evolu-
tionary sequences. A number of gener-
alizations, many of which are rather
speculative, and some of which may turn
out to be over-simplifications, have
been made. Probably, some of the
changes treated as if they were mono-
phyletic will turn out, on closer exami-
nation, to have been polyphyletic. On
the other hand, even if these changes
are polyphyletic, they are most likely
to occur in closely related forms, and
the trends may be expected to be inde-
pendent of those convergent or parallel
trends in other systems which confuse
the study of relationships. For these
reasons it is expedient to use, with
discretion, such a perhaps over-sim-
plified concept of the evolution of the
reproductive system within the group
for comparison of other lines of evi-
dence. It is hoped that the use of these
other lines of evidence will compensate
for the uncertainty and imperfection of
some of the lines of reasoning developed
above, and for any improbable evolution-
ary events (convergences) which may
have occurred. Four such kinds of
evidence will be used for consideration
of the validity of hypothetical relation-
ships suggested by the structure and
function of the reproductive system.
The first of these independent lines of
evidence is provided by previous syste-
matic work. A number of interrela-
tionships are well supported by inter-
mediate forms and by a large number
of agreements in details of structure,
and will be accepted. However, a
number of taxa have been erected only
for convenience, or are of disputed re-
lationship, especially those which are
highly modified and lack intermediate
forms, or have been based on simi-
larities likely to be convergent. There-
fore, an attempt has been made to draw
a “conservative” phylogenetic tree, em-
phasizing the placement of controver-
Sial groups only.
The second line of evidence willbe the
chromosome numbers, which, in spite
of our very imperfect knowledge, do
suggest some probable relationships.
Burch (1962) has noted that the chromo-
364 M. T. GHISELIN
some numbers of opisthobranchs are
quite constant in well-defined groups.
Inaba (1959), who reviews older work,
suggests a considerable divergence be-
tween the Acoela on the one hand, and
the Anaspidea, Sacoglossa and certain
Cephalaspidea on the other. He found
that in one species of Pleurobranchaea
the haploid chromosome number is 12,
while in 10 species of dorid nudibranchs
and 3 of aeolid nudibranchs, the haploid
chromosome number is 13; in the single
species which he examined in each of
the genera Aglaja, Philine, Petalifera,
Notarchus and Elysia, the haploid number
is 17. It is difficult to evaluate Zarnik’s
(1911) study of chromosomes in several
thecosomatous pteropods, since Inaba
(1959) found that most older counts are
inaccurate. Zarnik reports a haploid
number of 10 in one species, 12 in 2
others, and higher counts in various
other species. Equally difficult to
evaluate is the available information
on Haminoea; for one species Small-
wood (1904) gives a haploid number of
16, while Dupouy (1964) says that it
is 12 in a species with abnormal
meiosis.
The study of Franzen (1955) on the
morphology of the spermatozoon pro-
vides further evidence. He finds that
some opisthobranchs have spermatozoa
with long heads, while in others they
are short, the latter condition evidently
being primitive. Burch (1962) has ob-
served that Boettger’s (1954) phyloge-
netic tree is not consistent with the
sperm types. It appears that the phylo-
genetic relationships inferred in the
present study agree fairly well with the
oligophyletic origin of the long-headed
spermatozoon. The findings of Franzen,
supplemented by a few from the litera-
ture and some originalobservations, are
listed below.
Taxon
Cephalaspidea
Acteonidae
Acteon tornatilis
Philinidae
Philine aperta
P. scabra
P. alba
Aglajidae
Aglaja. sp.
Atyidae
Haminoea navicula
H. solitaria
Bullidae
Bulla gouldiana
Scaphandridae
Acteocina exima
Cylichna cylindracea
Diaphanidae
Diaphana minuta
Anaspidea
Akeratidae
Akera bullata
Aplysiidae
Aplysia punctata
Sacoglossa
Oxynoacea
Oxynoidae
Oxynoe sp.
Spermatozoa
Reference
Franzén, 1955
Franzén, 1955
Franzén, 1955
original
original
Dupouy, 1964
Smallwood, 1904
original
original
Franzén, 1955
Franzén, 1955
Franzén, 1955
Franzén, 1955
original
PHYLOGENY OF OPISTHOBRANCHS 365
Taxon
Elysiacea
Elysiidae
Elysia hedgpethi
Limapontiidae
Limapontia capitata
Stiligeridae
Hermaeina smithi
Thecosomata
Spiratellidae
Spiratella retroversa
Cavolinidae
Creseis virgula
Gymnosomata
Pneumodermatidae
Pneumoderma mediterraneum
Cliopsidae
Cliopsis grandis
Acochlidiacea
Hedylopsidae
Hedylopsis suecica
Entomotaeniata
Pyramidellidae
Partulida spiralis
Brachystomia ambigua
Nudibranchia
Doridacea
Onchidorididae
Onchidoris muricata
Dorididae
Archidoris tuburculata
Dendronotacea
Dendronotidae
Dendronotus frondosus
Tritoniidae
Tritonia hombergi
The phylogenetic arrangement used
here tends to put forms with similar
spermatoxoon morphology together, and
the same may be said of the chromo-
some numbers. However, it is impos-
sible to arrange the forms in such a
manner that the 2 criteria are com-
pletely consistent. It follows that suf-
ficient data are not yet available to
allow a complete synthesis, although the
results are encouraging.
A final line of evidence is speciali-
zation in diet. A number of opistho-
branchs are quite stenophagous andhave
a highly specialized feeding mechanism
or an unusual type of food. For example,
Spermatozoa
long
Reference
x original
x Franzén, 1955
x original
x Hsiao, 1939
X original
X Meisenheimer, 1905
X Meisenheimer, 1905
Franzén, 1955
Franzén, 1955
Franzén, 1955
Franzén, 1955
Franzén, 1955
Franzén, 1955
Franzén, 1955
the pyramidellids are all ectoparasitic,
the aeolid nudibranchs feed mostly on
hydroids, and all anaspideans and saco-
glossans are herbivores. A specialized
feeding mechanism may be considered
a complicated adaptive character com-
plex, which is not likely to be modified
into another specialized mechanism, and,
relatively speaking, is an irreversible
change. It is more reasonable to de-
rive organisms with different specialized
feeding mechanisms separately from
omnivorous or otherwise more gener-
alized feeders. The fact that unusual
exceptions exist to this general rule
does not invalidate the method, since
366 M. T. GHISELIN
E APLYSIIDAE ELYSIACEA
RUNCINIDA 11 OXYNOACEA
ATYIDAE AKERATIDAE 9 JULIACEA
a 8 10
BULLIDAE : CYLINDROBULLIDAE
ACOCHLIDIACEA —7 6
14 | 13 12 re DIAPHANIDAE
4
15 = >
PULMONA 1148 * THECOSOMATA
(INCLUDING
PHILINO- ONCHIDIIDAE) 3 ACTEON-
GLOSSIDAE IDAE GYMNOSOMATA
PYRAMIDEL- Е
RETUSIDAE LIDAE 2 An 19 7 UMBRACULIDAE
16 5 20
AEOLIDIACEA
Е Lee Kat PLEUROBRANCHIDAE 21 (POLYPHYLETIC)
SCAPHANDRIDAE He
DORIDACEA
AGLAJIDAE ) RS DENDRONOTACEA
ARMINACEA
GASTROPTERIDAE
FIG. 7. Phylogenetic tree showing inferred relationships in the opisthobranchs. Numbers refer
to discussion in text.
the hypothetical groups are considered
speculative unless supported by cor-
relation with other, independent lines of
evidence.
The results of an attempt to evaluate
the implications of the foregoing obser-
vations on opisthobranch reproductive
systems in the light of other lines of
evidence are given in the form of a
phylogenetic tree (Fig. 7), the numbers
on which refer to the discussions given
below. The diagram represents only the
inferred order of cladogenesis. Differ-
ent degrees of certainty are attached
to the various inferred relationships,
those which are most speculative being
accompanied by a question mark. In
view of the incomplete and sometimes
ambiguous evidence some rather arbi-
trary judgements have been made; hence,
somewhat different interpretations of the
phylogeny of the group could be ad-
vanced which are reasonably consis-
tent with the evidence.
1. Little else may be said about the
structure of the common ancestor of the
Euthyneura except that it had the typi-
cal euthyneuran spermatozoon, and that
it retained a number of “primitive” fea-
tures, such as an undivided gonoduct and
a streptoneurous nervous system. Whe-
ther or not to consider the common an-
cestor of the Euthyneura a member of
the Acteonidae is a matter of the defini-
tion of terms, but the presently existing
Acteonidae must be treated asa special-
ized branch which are not ancestral to
most other groups of opisthobranchs.
2. The Pyramidellidae show no par-
ticular similarities in the structure of
the reproductive system to any other
group of opisthobranchs, except that
their reproductive system can readily be
derived from the ancestral form of the
opisthobranchs in general. The rela-
tionship suggested here is based essen-
tially on the lack of evidence for an
affinity to other groups andis, of course,
PHYLOGENY OF OPISTHOBRANCHS 367
provisional. The theory of Boettger
(1954) that the pyramidellids are re-
lated to the Thecosomata finds no sup-
port in the structure of the reproductive
system; the presence of a shell and an
operculum in both groups is probably
due to the retention of primitive cha-
racteristics, or perhaps to neoteny in
the Thecosomata (cf. Lemche, 1948).
3. I agree with Solem (1959) in re-
jecting the notion of Fretter (1943) that
the Onchidiidae are opisthobranchs.
Fretter’s arguments are based onhighly
questionable premises, and anenumera-
tion of these follows. Her argument that
the Opisthobranchia and the Onchidiidae
agree in the loss of the shell and in
the reduction in size of the visceral
hump is beside the point, since such
a reduction in the shell and visceral
hump occurs in both pulmonates and
opisthobranchs. The posterior posi-
tion of the mantle cavity and the posi-
tion of the auricle behind the ventricle
in Onchidella could very easily result
from a posterior displacement of the
respiratory apparatus; there is no rea-
son for ascribing this displacement to
-opisthobranch affinities. Reduction of
the ganglia of the visceral loop in
Onchidella to 3 is not a sign of relation-
Ship to the opisthobranchs, since sucha
configuration occurs in such pulmonates
as Amphibola. The Onchidiidae can
scarcely be classified among the opistho-
branchs on the basis of their posses-
sion of 3 “liver” lobes, considering the
presence of a tripartite digestive gland
in Siphonaria, а marine pulmonate
(Marcus & Marcus, 1960a). Fretter’s
statement that the “general disposition
of the reproductive organs” in Onchi-
della agrees with that of opisthobranchs
is erroneous; the similarities to the
opisthobranch system are only of the
most general kind, such as would be
expected from both belonging to the
Euthyneura. The reproductive system of
the Onchidiidae agrees in general plan
with that of the Pulmonata (cf. Duncan,
1961), especially in the compact gonad,
the separation of the sperm-storing por-
tion of the ampulla from the conducting
part, the reduction of the receptaculum
seminis, the type of prostate, and the
only partial separation of the vas defe-
rens from the pallial gonoduct. The
presence in Onchidella of aveliger larva
is fully consistent with its pulmonate
affinities, since a veliger larva is pre-
sent in such pulmonates as Siphonaria
(Marcus & Marcus, 1960a). Arguments
that the lung is not homologous to that
of pulmonates are highly speculative
and questionable, because they are based
on a lack of embryological evidence;
direct development is highly likely, since
the lung develops late in ontogeny, and
the morphological position of the lung
is such that it could well have been
derived from a portion of the mantle
cavity. A comparison of the gastral
plates and tentacle-borne eyes to those
of prosobranchs is beside the point;
such a comparison, being based on simi-
larities which are not due to common
descent from an ancestor which posses-
sed these structures, does not do away
with the problem of a greater similarity
between the Onchidiidae and the Pul-
monata than between the Onchidiidae and
the Opisthobranchia. Iagree with Fretter
that the shortness of the visceral loop,
the closed vas deferens and the number
of lateral teeth on the radula are not
germane to the argument. Bergh’s
(1884) placement of the Onchidiidae in
the Pulmonata was based on a large
number of detailed agreements in the
structure of the nervous and digestive
systems in both groups. Boettger (1954)
related the Onchidiidae, in which the gan-
glia of the central nervous system tend
to fuse below the oesophagus, to the
pleurobranchs, in which the ganglia tend
to fuse above the oesophagus. On the
basis of his own criteria, it would seem
more consistent to relate the Onchi-
diidae to the pulmonates, in which the
ganglia show the same tendency to fuse
below the oesophagus, Ifthe Onchidiidae
are considered early derivatives of the
primitive Pulmonata, their similarities
to opisthobranchs are readily under-
368 M. T. GHISELIN
stood.
4. On the basis of the chromosome
evidence it seems reasonable to regard
the Thecosomata as a systematically
isolated group, but I see more sound
evidence for relating the Thecosomata
to the Gymnosomata than for relating
either group to any other opisthobranchs.
Pelseneer (1888) is largely responsible
for the prevalent opinion that the Gymno-
somata are derived from highly-special-
ized Anaspidea and the Thecosomata
from some unspecified group of Cepha-
laspidea. The reason for relating the
Thecosomata to the Cephalaspidea was
the retention of numerous characteris-
tics, such as a relatively unconcentrated
nervous system, gizzard plates and the
like, which characterize the cephalaspi-
deans; yet he gave no evidence to show
that the Gymnosomata were not derived
from such a cephalaspidean, or that the
modern pteropods were not derived from
a commonancestor which was a pteropod.
Pelseneer did manage to find some
characteristics in common between the
Gymnosomata and Anaspidea. Inthe first
place, the nervous system shows the
same kind of concentration; yet the ner-
vous system is concentrated only in the
most highly modified anaspideans, so
one must reason either that the simi-
larity is convergent and beside the point,
or that an exceedingly specialized, mo-
dern form gave rise, directly, to the
order Gymnosomata. One cannot, as did
Boettger (1954), derive the gymnoso-
matous pteropods from the primitive an-
aspideans and support this relationship
on the basis of the structure of the
nervous system. The other significant
similarity is the supposed homology be-
tween the pharyngeal hooks of the anas-
pideans and the hook-sacs of the gymno-
somatous pteropods, a homology open to
question and also referable to a common
ancestry between the 2 groups at a much
earlier stage than that envisioned by
Pelseneer. Morton (1958) rejects this
homology, but only on the lack of de-
tailed agreement; a more sound, but not
compelling, argument is the complete
absence of either of these cuticular
structures in such “primitive” forms
as Hydromyles, a discrepancy which
Hoffmann (1932-40) rationalizes as
secondary.
On the basis of similarities between
the tentacles of both orders of ptero-
pods, in which the posterior pair of
tentacles bears an eye, Hoffmann (1932-
40) denied a homology between the ten-
tacles of gymnosomatous pteropods and
anaspideans, and suggested relating both
groups of pteropods to an early pre-
cursor of the Anaspidea. Again, if such
an inference is made, then the similari-
ties in nervous systems no longer apply.
Meisenheimer (1905) affirmed the homo-
logy between the “wings” inthe 2 groups;
this homology may be supported on the
basis of conditions which occur in the
“primitive” gymnosomatous pteropod
Hydromyles, which resembles the theco-
somatous pteropods more than most
other members of its order (cf. Tesch,
1950). It is very difficult to derive the
“wings” of gymnosomatous pteropods
from the reduced epipodia of higher
anaspideans.
Of some interest is the theory that
the Thecosomata are neotenous Cepha-
laspidea, a theory supported by the sin-
istrality (hyperstrophy) of the larval
shell among Opisthobranchs in general,
some of the Basommatophora, and in
some adult Thecosomata. Neoteny would
provide a simple means of reducing
the size of the body in adaptation to
the pelagic habitat, and has been re-
ported in some Gymnosomata (Danforth,
1907). Their manner of origin, how-
ever, reveals little concerning their
relationships.
Minichev (1963), after studying the
central nervous system of Hydromyles,
has concluded that the similarities it
bears to that of the higher Anaspidea
are due to convergence; this conclusion
seems reasonable in view of the de-
tailed structure. He derives the Gymno-
somata from the Akeratidae and the
Akeratidae from the Acteonidae, while
treating the Thecosomata as separately
PHYLOGENY OF OPISTHOBRANCHS 369
derived from the Acteonidae. Yet he
gives no compelling reason for sepa-
rating the 2 groups, although he does
point out that there are many differences
between them and that convergence could
account for the similarities. His notion
that either group could be derived from
the Acteonidae is not supported by argu-
ments, and he gives no explicit reasons
for relating the Gymnosomata to the An-
aspidea. Nor does he provide any argu-
ments against the possiblity that the 2
orders are related, but diverged at an
early stage in their evolution.
Aside from the inconclusive chromo-
some evidence, the most consistent in-
terpretation would be to consider the
pteropods monophyletic and members of
the same clade as the Anaspidea, but
by no means derived from them. This
intepretation is supported by the evidence
from spermatozoon morphology. The
hook-sacs, tentacles and reproductive
systems would then be explained, and
differences between the 2 orders of
pteropods would make sense as diver-
gences largely related to different
feeding mechanisms.
9. The placement of Anaspidea, Saco-
glossa and the more typical Cephalas-
pidea in a single clade rests largely
on the admittedly incomplete chromo-
some evidence mentioned above. There
is no compelling morphological evidence
for this relationship, but neitheristhere
any against it.
6. This clade (Sacoglossa, Anaspidea,
Diaphanidae and perhaps the Acochli-
diacea) is based on the tendency for the
prostate to remain pallial and the gono-
duct to be oddiaulic. It appears that
the absence of well-developed gizzard
plates in this group is a primitive trait,
since the projections in the gizzard
of anaspideans show similarities to the
cuticularizations found in that of the
Diaphanidae (Odhner, 1926), rather than
to the well-developed, opposed plates
found in such forms as Haminoea and
Scaphander. The pteropods likewise
appear to have diverged at a stage when
the gizzard plates were not well de-
veloped.
7. In the absence of clear-cut evi-
dence to the contrary, I accept Odhner’s
(1952) idea that the Acochlidiacea are
related to the Diaphanidae, with the
reservation that small size, convergence
and the retention of primitive traits
might easily lead one to infer that these
forms are more closely related than
is actually the case. Indeed, the pre-
sence of elongate spermatozoon heads in
the Diaphanidae, Sacoglossa and Anas-
pidea, rather than short ones as in the
Acochlidiacea (Franzén, 1955) strongly
suggests that the Acochlididacea are not
closely related to the Diaphanidae, and
such an interpretation would be consis-
tent with the anatomy of the repro-
ductive system.
8. Not enough is known of the inter-
nal structure of the Diaphanidae and their
close relatives to determine their exact
relationships, especially since some ap-
pear to be rather reduced in size. The
nervous system in the Diaphanidae is
highly primitive, and nothing in its
structure would preclude such a type
serving as an ancestral form for the
other members of the clade, such as
the Acochlidiacea, Anaspidea or Saco-
glossa (cf. Odhner, 1926). Odhner (1926)
was the first to suggest a unity of these
forms on the basis of the structure of
the pallial gonoduct. Marcus & Marcus
(1956b) have shown that Cylindrobulla
shows characteristics suggestive ofboth
the Anaspidea and the Sacoglossa. The
major distinction between the reproduc-
tive systems of the anaspideans and the
sacoglossans is that of the copulatory ap-
paratus, which does not include a closed
ejaculatory duct in the Anaspidea; the
absence of such a closed ejaculatory
duct in Colobocephalus suggests that the
Diaphanidae may well have been an-
cestral to the Anaspidea. Of great
interest is the fact that both the Saco-
glossa and the Anaspidea are herbivo-
rous, and this similarity may well have
resulted from descent from an herbi-
vorous common ancestor.
9. The placement of the Akeratidae
370 M. T. GHISELIN
among the Anaspidea (Guiart, 1901) is
well supported by the structure of the
reproductive system, as well as by nu-
merous other similarities, and is no
longer disputed.
10. Cylindrobulla is here considered
a sacoglossan. Its ejaculatory duct
may be looked upon as an early stage
in the complete separation of the vas
deferens of higher sacoglossans. The
uniserial radula, which admittedly may
be convergent due to small size, is a
characteristic feature of the Sacoglossa.
Marcus & Marcus (1956b) have shown
some similarities in the radula of Cylin-
drobulla to that of the Diaphanidae.
11. The polyphyletic derivation of the
shell-less sacoglossans from the shelled
ones as suggested by Boettger (1954)
appears likely. However, I follow Baba
(1961) in assuming that the Oxynoidae
and Juliidae are closely related forms
which are not ancestral to the shell-
less sacoglossans; they could easily be
derived from other shelled sacoglossans.
The single split in the oviduct is an
ancestral characteristic of the Saco-
glossa, and therefore a poor indication
of the relationships within the group;
however, in future studies it may be
of value to consider the possibility of
a relationship between Hermaeina and
Alderia, in which there is only a single
split. The similarity in pattern of the
first split in the oviduct of Elysia to
the single one in Caliphylla likewise
suggests a possible relationship. The
peculiar construction ofthe reproductive
system in Limapontia and a number of
other forms can easily be derived from
conditions found in Elysia, and a re-
lationship is at least possible. Aproper
conception ofthe relationship between the
various groups of sacoglossans must
await precise knowledge of the details
of the reproductive system in other
forms. However, sufficient evidence
is available to show that the repro-
ductive system throughout the group
has the same fundamental organization,
and the suggestion of Gascoigne (1956)
that the Sacoglossa are polyphyletic must
be considered quite dubious.
12. All members of the Cephalas-
pidea except those allied to the Acteoni-
dae or to the Diaphanidae are here
united in a single clade. The pre-
sence of well-developed gizzard plates,
few in number and opposed to each
other, is wide-spread among these
forms, and probably represents an in-
heritance from the common ancestor of
the clade. The gizzard plates seem
to be absent mostly in forms with a
specialized feeding mechanism, or in
those which are minute (e.g. Philino-
glossa). The reproductive system, es-
pecially the copulatory apparatus, is
derivable from a common type. Simi-
larities in general structure between
some Scaphandridae and Retusidae like-
wise suggest an affinity (cf. Lemche,
1948).
13. This clade, (Retusidae, Philino-
glossidae, Bullidae, Atyidae and Run-
cinidae) which may be polyphyletic to
some degree, includes all forms in
which the copulatory apparatus includes
a prostate and stores sperm.
14. The Bullidae, Atyidae and Run-
cinidae are united partly on the basis
of their herbivorous habits (Pruvot-Fol,
1954; Guiart, 1901; Ghiselin, 1963). They
all, with the possible exception of Ham-
inoea, possess an oesophageal diverti-
culum which is probably homologous
within the group, but the significance
of which has been overlooked (cf.
Hoffmann, 1932-40). This diverticulum
is present in Bulla (Pelseneer, 1894),
Phanerophthalmus (Eales, 1938), and
Runcina (Ghiselin, 1963). I have found
no record of an equivalent structure in
the Anaspidea, pteropods, Scaphandridae
or Philinidae. But since a similar
structure is present in Diaphanidae and
Sacoglossa, this diverticulum may be a
primitive trait which is retainedin some
herbivorous forms; the possibility that
it is homologous to the oesophageal
glands of prosobranchs, thought to be
absent in opisthobranchs (Fretter &
Graham, 1962) should be investigated.
The Bullidae are more primitive than
PHYLOGENY OF OPISTHOBRANCHS 371
other members of this groupin degree
of loss of the shell, of development of
nervous concentration and of integration
of the gizzard apparatus, and may have
diverged early. Boettger’s (1954) idea
that the development of a posterior posi-
tion of the nerve ring in the Atyidae
and Runcinidae is convergent, however
true the idea itself may be, was in-
consistent with his own phylogenetic
method. Marcus (1957) has shown that
a derivation of the nervous system in
the Runcinidae and Atyidae from that of
the Bullidae is fully consistent with the
conditions of the nervous system in Bulla.
Yet he used this sequence to show that
the nervous system is not a good source
of indications of relationships, since he
was unable to see any reasons for re-
lating these forms. Resemblances of
Випста to the Notaspidea are, as
Pelseneer (1894) demonstrated, super-
ficial only.
15. The relationships between the
Retusidae and Philinoglossidae are un-
clear. I agree with Boettger (1954)
in relating the Retusidae (including Rhi-
zorus) to the Bullidae and Atyidae, but
‘the groups are so ill defined as to
scarcely warrant precise statements as
to their relationships. The peculiarities
of the Philinoglossidae, however much
they make relationships uncertain, are
clearly due to reduced size, and do not
necessitate the erection of a new order
as proposed by Odhner (1952). Simi-
larly, any relationship to the Acochli-
diacea, as suggested by Pruvot-Fol
(1954), must also be rejected as based
on convergence, as Pruvot-Fol herself
implies.
16. The structure of the reproductive
system bears out the concensus of
workers in the field that the Philinidae,
Scaphandridae, Aglajidae and Gastrop-
teridae are interrelated. I use the
term Scaphandridae to include the genera
Scaphander, Cylichna, Cylichnella, Ac-
teocina, and doubtless some other forms
which cannot yet be placed, since their
anatomy is poorly known. It seems
more prudent to consider the Philini-
dae, Aglajidae, and Gastropteridae as
independent derivatives from a primi-
tive stock than to attempt to relate
any of these families to one another,
since a considerable amount of parallel
evolution has evidently taken place.
17. If we accept the authority of
Eliot (1910) on the structure of the
reproductive system in Umbraculum,
then all members of this clade possess
a reproductive system which is andro-
diaulic or else is derived from sucha
one. The similarity between the am-
pullae is at least suggestive. Eliot
(1910) notes a number of other simi-
larities which imply that there is an
affinity between the Acoela and the
Hydatinidae and Acteonidae, although
the degree of divergence since clado-
genesis would appear to have hindered
the acceptance of his interpretation.
Likewise a typological outlook would tend
to require the placement of Acteon as
it presently exists at the base of the
evolutionary tree ofthe Opisthobranchia.
If one thinks of the Acoela as related
to one group of somewhat aberrant forms
bearing a close resemblance to those
Acteon-like forms which evidently gave
rise to other opisthobranchs, then there
is nothing unreasonable about the rela-
tionship which Eliot suggested.
18. The unique features of the repro-
ductive system which set the Acteonidae
and Hydatinidae off from the rest of
the opisthobranchs can scarcely be at-
tributed to convergence alone. Thus
cladogenesis between these 2 families
took place after they acquired these
features, and an isolated position for
them is essential. These families are
rather similar in general anatomy, and
it appears that both the Acteonidae and
Hydatinidae are specialized feeders on
annelids (Eales, 1938; Marcus, 1956).
Boettger’s (1954) placement of the Hy-
datinidae and Acteonidae, with the Ac-
teonidae ancestral to all Euthyneura and
the Hydatinidae related to the Diaphani-
dae, is not consistent with the fact that
in both the Acteonidae and Hydatinidae,
the cerebral and pleural ganglia are
372 M. T. GHISELIN
intimately fused.
19. The Umbraculidae are here treated
as a specialized side branch within the
Notaspidea; not enough is known of their
reproductive systems to allow precise
placement, and it may well be that
their conchological similarities are con-
vergent. Boettger (1954) considered the
Umbraculidae ancestral to the Nudi-
branchia, and the Pleurobranchidae an
early, unrelated offshoot, reasoning on
the basis of the somewhat more con-
centrated nervous system in the Um-
braculidae, but parallelism easily ex-
plains this.
20. Relationships between the various
notaspideans will not be discussed here.
A sufficient range of variation in the
anatomy of the reproductive and nervous
systems exists in the pleurobranchs to
allow the derivation of the nudibranchs
from them. The idea of Boettger (1954)
that the Dendronotacea are more closely
related to the Doridacea than to the
Aeolidiacea and Arminacea should be
rejected as based on the common re-
tention of a number of primitive charac-
teristics inherited from the pleurobranch
common ancestor of the Nudibranchia.
The Dendronotacea show numerous fea-
tures of their anatomy which link them
closely to the Arminacea and Aeolidi-
acea. It seems, however, that many fea-
tures held in common by aeolid nudi-
branchs, particularly those of the diges-
tive system, are due to parallel adapta-
tions to the same kind of food, i.e. to coe-
lentrates. But the correlation between
diet and the details of structure of the
reproductive system strongly suggests
the unity of the aeolid nudibranchs as a
Single clade, although the common an-
cestor of the group may well have been
a pleurobranch.
21. The most widely accepted division
of the aeolid nudibranchs into systematic
groups is that of Odhner (1934, 1936,
1939), who has distinguished the Dendro-
notacea, Arminacea and Aeolidiacea on
the basis of external morphology andthe
tendencies of differentiation of the gut.
The Dendronotacea are thought to be the
most primitive of the aeolid nudibranchs,
some of them possessing a number of
characteristics, such as a velum, back
margin and only partially divided diges-
tive gland, which are thought to be de-
rived from notaspidean ancestors
(Odhner, 1939: 24). The Aeolidiaceaare
characterized by a gradual loss of notas-
pidean characteristics, with progressive
development of several evolutionary
trends. These trends include: (1) rami-
fication of the digestive gland, (2) de-
velopment of cerata, (3) loss of the velum
and its transformation into tentacles,
(4) reduction of rhinophore sheaths, (5)
shortening of optic nerves, (6) displace-
ment of the anus toward the dorsal
surface. These trends also occur in the
Arminacea and Dendronotacea. Odhner
has based his classification in part on
the degree of development of such
changes and in part on various diver-
gences in structure which can be re-
lated to them. His system is widely
accepted, and does seem to reflect
relationships. However, the present
study suggests some possible improve-
ments. Thompson (1961a) has pointed
out the importance of the larval shell
in the classification of the aeolid nudi-
branchs. It would seem that the only
member of the Dendronotacea which has
a larval shell of type two, Dendronotus,
is the only member of the Dendrono-
tacea which has a triaulic reproductive
system. Unlike all other Aeolidiacea,
the Acleioprocta have a larval shell of
type two. The Acleioprocta include some
forms which are evidently diaulic, such
as Eubranchus (Lloyd, 1952) and Calma
(Evans, 1922), but a number of others
are triaulic, such as Pseudovermis
(Marcus & Marcus, 1955b), Miesea
(Marcus, 1961a), and Embletonia
(Marcus, 1957; Chambers, 1934; Marcus
& Marcus, 1955b). The fact that these
triaulic forms are small and aberrant
and do not fit well into Odhner’s scheme
of classification (Embletonia has afron-
tal veil) deserves careful consideration
by systematists, for it strongly suggests
that the Aeolidiacea are polyphyletic.
PHYLOGENY OF OPISTHOBRANCHS 373
ACKNOWLEDGEMENTS
I wish to express my deepest grati-
tude to Dr. Donald P. Abbott for his
inspiration, assistance and direction
during the course of this study.
For providing some of the specimens
used, I thank Drs. L. R. Blinks, J. A.
McGowan, J. H. McLean and J. H.
Dearborn.
Support during the period of research
was provided, in part, by United States
Public Health Service Training Grant
5-TI-GM -647.
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RESUMEN
FUNCION REPORDUCTORA Y FILOGENIA DE GASTROPODOS OPISTOBRANQUIOS
La anatomia comparativa y funcional del sistema reproductor en toda la subclase
Opistobranchia se trata criticamente con la finalidad de proveer una base mas sölida
para estudios filogenéticos. Observaciones originales se combinan con discusiones
detalladas de otros trabajos, dando especial importancia a posibles explicaciones
funcionales de las variaciones morfolögicas y fisiolögicas, que conduzcan a una teoria
filogenética con base causal. En el analisis de las funciones se evita la consideración
de aspectos que tienen la posibilidad de ser convergentes, destacando la comparación
basada en complejas divergencias funcionales.
La homología de las partes es tratada en detalle y se sugieren algunos cambios en
nomenclatura. La formación de masas ovígeras y las homologías de las glándulas que
las producen, se discuten y clarifican por observaciones experimentales e histo-
química.
Se consideran las posibles razones de los cambios evolutivos. Desventajas fun-
cionales de los gonoductos de caracter ancestral, no divididos, se han superado en
diferentes maneras, y tales divergencias dan base para hipótesis que se evaluan en
términos de otras evidencias.
También se consideran trabajos sistemáticos anteriores, numero de cromosomas,
especialización alimenticia y otras propiedades del sistema digestivo, y la morfo-
logía espermatozoica, como evidencia auxiliar en la discusión de problemas filo-
genéticos, los cuales incluyen consideración crítica de paralelismo y convergencia.
El sistema reproductor de los Ochidiidae mantiene afinidades con pulmonados.
Los Acteonidae tienen un sistema reproductor modificado y no son ancestrales a la
mayoria de otros opistobranquios, y aquel, asi como otras estructuras implican una
estrocha relación con los Hydatinidae; la histología de la ampolla sugiere posible
afinidad con los Acoela. Se rechazan otras premisas sobre las cuales se habian
basado argumentos para un origen bifiletico de los Pterópodos; su origen monofiletico
es consistente con la morfología del sistema reproductor; ambos grupos se asemejan
a los Anaspidea y Sacoglossa en morfología espermatozoica. El sistema reproductor
de Anaspidea, Sacoglossa, Diaphanidae y Cylindrobullidae pueden compararse a un ап-
tecesor común hipotético con un gonoducto dividido, y pueden estar relacionados. Los
Retusidae, Philinoglossidae, Bullidae, Atyidae y Runcinidae pueden agruparse juntos
en base al aparato copulador el cual almacena esperma y forma espermatóforos;
miembros herbívoros de este grupo tienen un divertículo esofágico y similaridades en
la molleja. Correlaciones entre tipos de concha larval y la condición triáulica en
nudibranquios aeolidos sugieren una necesidad de revisión sistemática. El estudio
soporta la naturalidad de muchos grupos.
Verh.
MALACOLOGIA, 1966, 3(3): 379-398
A CONTRIBUTION TO THE CONCHOMETRY OF
BIOMPHALARIA PFEIFFERI (BASOMMATOPHORA: PLANORBIDAE)
G. H. Frank and A. H. Meyling
Council for Scientific and Industrial Research
Pretoria, Republic of South Africa
ABSTRACT
The shell of Biomphalaria pfeifferi, in common with many molluscs, is in the
form of a logarithmic spiral, its idealized shape being close to its actual shape.
Equations based on this fact were used to calculate its surface area and its
weight per square millimeter. As a check, estimationsby a more direct method
were done and found to be in substantial agreement. Results based on shells
from natural and artificial habitats suggest that the average weight per square
millimeter increases with age and with increase of soluble calcium in the
medium. This increase apparently takes place equally in all parts of the shell,
i.e. the weight per square millimeter for any part is approximately equal to the
average measurement for the whole shell. It would appear that the valuekj
(radius of whorl/radius of spiral at that point), or its equivalent ratio, shell
height to maximum shell diameter, decreases with age and with an increase in
the aggressive carbon dioxide of the habitat. If, as the results of this limited
investigation suggest, the shell of Biomphalaria always approximates the ideal-
ized shell form, detailed conchometry by conventional methods is unnecessary.
Full mathematical analysis would only be required if it were found that the rate
(1) at which the whorls recede from the centre and the aperture diameter (re-
lated to тф ) in similar size groups were significantly different.
INTRODUCTION
It is now well established that the
mineral substances for shell formation
in aquatic molluscs may be derived
directly from the water of the natural
habitat (Galtsoff, 1934; Robertson, 1941;
Raven, 1958; Jodrey, 1953). Anadequate
concentration of these saltsinthe habitat
is therefore of some importance to the
snail. As a preliminary towards a
better understanding of the role of dis-
solved calcium in the biology of Biom-
phalaria pfeifferi (Krauss), it was con-
sidered of value to discover whether
variation in the concentration of this
salt in the water of the natural habitat
had any direct and easily detectable
influence on the shape and thickness
of the shell.
An attempt was made to measure
thickness directly with an eyepiece
micrometer after grinding the shell into
thin sections, but, due to the sculpturing
of the shell surface and the difficulty
of orientating the edge to be measured
accurately, the technique was found im-
practical at the high magnifications re-
quired. Since the shell was found to be
considerably thicker in the immediate
vicinity of the sutures, a large number
of measurements would also have been
required to arrive at a satisfactory
average value. In addition none of these
measurements would have revealed any
variations in the form of the shell.
Because of these difficulties a mathe-
matical analysis of shell-form was
attempted in order to calculate the sur-
face area and, from it and the total
weight of the shell, to derive an average
value for the weight per unit area. As
far back as 1838, Moseley had demon-
strated that the shell of Nautilus was
a logarithmic spiral, and soon after-
wards, that this was also true of all
(379)
380 FRANK AND MEYLING
TABLE 1.
No. of determinations done
Colour (APHA units)
Turbidity (ppm SiO»)
pH
Conductivity (micromhos)
Alkalinity (ppm CaCOg)
Calcium (ppm CaCO,)
Magnesium (ppm CaCO3)
Iron (ppm Fe)
Manganese (ppm Mn)
Chloride (ppm Cl)
Sulphate (ppm SO4)
Silica (ppm $105)
Ammonia (ppm N)
Albuminoid amm. (ppm N)
Nitrites (ppm N)
Nitrates (ppm N)
Phosphates (ppm PO,)
Oxygen absorbed (4 hrs, ppm 0)
Aggressive CO, (ppm СО5)
Na and K (calculated)
spiral ammontoid and gastropod Mol-
lusca (from d’Arcy Thompson, 1917).
His ideas were taken up and elaborated
by Blake in 1878 and d’Arcy Thompson
early in the present century. Subse-
quently Huxley (1932) was able to show
that, in simple accretionary growth such
as that of the molluscan shell, a regular
gradient in the growth-rate across the
shell-forming organ (i.e., mantle edge)
must of necessity produce a structure
which is basically of a logarithmic spiral
form. He was also able to show that
these gradients in growth-rate per-
meated the entire organism (so-called
cortical field) and varied regularly not
only antero-posteriorly but also later-
ally, but expressed themselves only in
certain competent areas. Thus, in the
veliger of Haliotis, although the shell is
Physico-Chemical analysis of waters from 5 habitats
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at first cup-shaped, asymmetry is al-
ready present in the neighbouring soft
parts (e.g. liver) and it is this asym-
metry of the soft parts which determines
the shape of the shell (Eales, 1950). A
purely speculative suggestion based on
Huxley’s theory of growth gradients is
that the almost bilaterally symmetrical
shell of Biomphalaria must be looked
upon as arising from a mantle edge which
is primarily median in position with its
growth gradient diminishing antero-
posteriorly. The turbinate spiral shell
of Bulinus on the other hand is formed
by a laterally situated mantle edge with
its growth gradient diminishing not only
antero-posteriorly but also laterally, the
latter gradient being responsible for
the ‘shear’ in the shell spiral. That
a laterally situated mantle edge (brought
EEE
CONCHOMETRY OF BIOMPHALARIA 381
about by the process of torsion) will
produce this particular type of shell
is indirectly supported by Raven’s re-
mark (1958) that when “coilingby unequal
growth of the shell begins before torsion
it takes place according to the plane of
symmetry” (e.g. in Trochus) and that
the asymmetrical coiled shell forms only
after torsion has taken place (e.g. in
Haliotis). Torsion of the rapid type
brought about by the contraction of the
velar retractor muscle (e.g. early tor-
sion in Haliotis or later torsion in
Acmaea) apparently does not affect this
bilateral symmetry.
ORIGIN OF MATERIAL
Wild Snails. Four widely separated
habitats, in which the average dissolved
calcium content ranged from approxi-
mately 5-115 ppm were chosen and a
single graded series (from about 2-10
mm) of 20 undamaged shells was selected
from each. In addition 20 shells from
snails bred in outdoor aquaria at the
laboratory were also used. Collections
were not made at the same time of the
year.
The physico-chemical characteristics
of these 5 waters are given in Table 1.
However, as Macan (1950) has shown,
such general analyses seldom give more
than a rough picture of actual conditions
in the microhabitat. Joubert’s Dam is a
small catchment reservoir in a moun-
tainous, soft-water area. Shiya-lo-
Ngubu Dam is similarly situated but is
far larger and about 1,000 ft higher.
Both Buffelspruit and Ngwetispruit are
hard-water streams (Schutte & Frank,
1964) flowing off the Jamestown Igneous
Complex. Shells from Joubert’s Dam
often showed severe erosion of the inner
whorls, probably due to the action of
aggressive carbon dioxide which was
found to be over 8 ppm there. The
Shells selected for this investigation
were, however, relatively undamaged.
Most of the total hardness of the
waters of this area is due to magnesium
(expressed as CaCO3 in Table 1). Mag-
nesium carbonate, which is much more
soluble than the Ca salt, is not likely
to contribute to shell structure (Frank,
1963) and has therefore been ignored in
our evaluations.
Laboratory Snails. Because it is
quite probable that the snails from these
5 habitats, although nominally all of
the same species, had very different
genotypes (Paraense, 1956), andbecause
it was also impossible to separate the
effect of the aggressive carbon dioxide
in the natural habitat from that of
calcium, it was thought advisable to
breed snails in the laboratory under
varying experimental conditions. Four
groups of eggs, all originating from the
same inbred laboratory stock, were
therefore exposed to 4 different com-
binations of calcium carbonate and
aggressive (free) carbon dioxide, pro-
ducing variable amounts of dissolved
calcium bicarbonate. Upon hatching,
the young snails were cultured in these
media for a further 15 weeks under con-
ditions very similar to those described
in a previous paper (Frank, 1963). Ten
snails were kept in one litre of medium,
with 4 aquaria to each of the 4 different
media. But, as difficulty had been
experienced before on bubbling air
through the aquaria, it was not attempted,
this time, to pass the experimental
gaseous mixtures through the culture
aquaria directly. The different experi-
mental media were prepared separately;
they were brought to equilibrium with
their air-carbon dioxide mixtures for
24 hours before being siphoned, with a
minimum of agitation, into the aquaria.
The media were changed daily and the
snails fed freshly scalded lettuce and
lucerne.
Conditioned tap water, the same as
that used in the outdoor aquaria (Table
2) but slightly diluted with glass distilled
water, was used to make up the experi-
mental media. Excess calcium carbon-
ate (approx. 2 g/l) was added to 2 of
the experimental media (C and D). Air
from which the carbon dioxide had been
partially removed, was passed through
382 FRANK AND MEYLING
TABLE 2. Mean and range of conditions* to which snails were exposed in experimental media.
Aquarium conditions
Reduzdd Mean 24.5 ppm
co Max. 32.3 ppm 34.
2 Min. 21.2 ppm
Exa Mean 24.7 ppm
co Max. 34.0 ppm
2 Min. 20.8 ppm
No free CaCO3
*From 9 determinations
2 media, A and C, (the latter with and
the former without excess calcium car-
bonate) until equilibrium was reached.
Another stream of air, enriched with
carbon dioxide, was passed through the
other 2 media (B and D) also until
equilibrium had been reached.
The air with reduced carbon dioxide
content was simply prepared by passing
it through a column of soda-lime. To
make a COo-enriched air mixture of а
reasonably stable composition, a stream
of air was first dried in a silica gel
column and then passed through a 25%
constant boiling mixture of water and
hydrochloric acid kept at roughly 30°C in
a water bath. This acidified air was
then passed through a saturated solution
of sodium bicarbonate, where it became
neutralized and picked up CO». Since a
constant boiling hydrochloric acid-water
mixture evaporates (at constant temper-
ature) at afixed rate, an air-COy mixture
of constant proportions can thus be pro-
duced. By holding the acid at a higher
or lower temperature more or less
carbon dioxide can be produced.
Calcium concentration
at beginning
h
er 24
rs
24.2
19.6
23.3
35.6
16.8
52.8
69. 2
44.6
E Rediiéed Mean 33.1 ppm
2 Max. 40.8 ppm
Et | CO2 1
Mo N Min. 29.2 ppm
an
Ф
7 Extra Mean 89.6 ppm 107.7
El 60 Max. 119.2 ppm | 157.0
- Min. 55.2 ppm 68.4
Aggressive CO,
concentration
hrs
Overall mean
2.9 7.3
4.6 9.5 24 ppm 5.1 ppm
10 5.0
8.9 qos
12.0 329 24 ppm 8.4 ppm
5:1 6.3
0. 85 2.5
5.3 4. 6 43 ppm
0.0 0.5
98 ppm
No attempt was made to measure the
concentrations of carbon dioxide in the
mixtures directly as this was relatively
unimportant in the context. Although
the media were renewed every day, the
content of aggressive carbon dioxide and
dissolved calcium was determined
weekly for the first 9 weeks only. In all
9 pairs of determinations were done:
one immediately before addition of the
media to the aquaria and another 24
hours later, i.e. just before they were
discarded. The results are summarized
in Table 2. The aggressive carbon
dioxide in the samples was determined
by agitating the sample at intervals,
for 24 hours, out of contact with the
air, with an excess of calcium carbon-
ate: the concentration of aggressive
carbon dioxide was then calculated from
the increase in soluble calcium bicar-
bonate found. All calcium determin-
ations were done by the well-known
versenate method.
The following should be noted in regard
to Table 2.
(1) Media poor in calcium carbonate.
CONCHOMETRY OF BIOMPHALARIA 383
Since there was little calcium in medium
A to act as buffer, aggressive conditions
developed as soon as the carbon dioxide
from the snail metabolism found its
way into the water. The carbon dioxide
mixture passed through medium B made
it very aggressive indeed, butthisinitial
condition slowly abated after the medium
was placed in the aquaria and the excess
carbon dioxide was able to diffuse away.
(2) Media with excess calcium carbonate.
Medium D and especially C never had
much aggressive carbon dioxide present,
since it was immediately taken up by
the free calcium carbonate which was
then converted to the more soluble cal-
cium bicarbonate. The concentration of
soluble calcium rose steadily during the
period the snails were in the medium.
(3) Presence of carbon dioxide in soda-
lime treated air.
As a litre of water at room temperature
will only dissolve about 14 mg of cal-
cium carbonate without the assistance
of carbon dioxide and as the initial mean
content of soluble calcium in medium C
was about 33 ppm and that of medium
A was 24.5 ppm, we must conclude that
the soda-lime columns failed to remove
ali the carbon dioxide from the air
streams conditioning these 2 media.
Although the limited facilities avail-
able did not enable us to maintain rigidly
constant conditions, the results of their
effect on shell growth were sufficiently
significant to confirm and further illus-
trate our field findings.
METHOD
In any individual adult shell of Biom-
phalaria pfeifferi it may be shown, by
comparing the ratios of the diameters
of each whorl with its successor, that
it is in the form of a logarithmic spiral.
Unfortunately, because there is a slight,
almost regular increase in the ratios as
the apex of the shell is approached, the
idealized form upon which the equation
is based is not valid for the very young
snail. Waddington (1929) founda similar
condition in Ammonites and worked out a
BIG. val
sagittal section to show how the 3 largest
diameters (a, b and c) were measured (in
mm).
Shell of Biomphalaria pfeifferi in
correction factor for it. Because the
innermost whorls were difficult to
measure accurately and since it could
be shown mathematically (Appendix 2)
that the surface area of the last whorl
of the shell was approximately 4 times
greater than that of the rest of the shell,
it was decided there was little loss in
accuracy when the mean of only 2 ratios
(derived from the last 3 whorl diameters)
was used in the subsequent calculations.
The equation for shell form and the
reasoning which led to its formulation
is given in Appendix 1.
All shells were carefully cleaned in
a very weak solution of caustic potash
to clear them of residual organic matter.
After thorough drying they were immer-
sed and cleared in toluol. This makes
it possible to take measurements of the
internal structure without destroying
the shell. With a low-power eyepiece
micrometer the 3 largest spiral dia-
meters lying on a line passing through
the centre of the shell and the outer
edge of the aperture (Fig. 1) plus the
average of 3 readings of the diameter
of the aperture (taken at right angles
384 FRANK AND MEYLING
NCGWETISPRUIT
114 ppm Ca
2130
Е OUTDOOR AQUARIA
x 37 ppm Ca
5
я
a SHIA-LO-NGUBU DAM
& 5 ppm Са
a
>
<
x 20
= BUFFELSPRUIT
3 82 ppm Ca
=
m
JOUBERTS DAM
4 ppm Ca
——
4 6 8 10 12
Q - MAXIMUM DIAMETER IN MM
FIG. 2. Relationship between shell size and its average weight per square millimeter in
different natural habitats.
to the walls) were determined.
A summary of the calculations per-
formed to arrive at the average weight
per square millimeter in an individual
shell may be found in Appendices 1 and
3.
RESULTS
Average weight per square millimeter.
On calculating the average weight per
square millimeter for each individual
shell in each natural habitat group it
was found that this dimension gradually
increased with an increase in the size
of the shell. For each habitat the most
probable curve (by least squares) repre-
senting this increase was found to be,
Joubert’s Dam:
у = 0.0960 + 0.00489a + 0. 00096322
Shiya-lo-Ngubu Dam:
У = 0.0415 + 0.0157a + 0. 000420a2
Outdoor Aquaria:
y = 0.0985 - 0.006582 + 0. 00234a2
Buffelspruit:
y = 0.0465 + 0.0104a + 0. 000314а2
Ngwetispruit:
у = -0. 235 + 0. 0751а - 0. 0021322
where у is the average mg/mm2and а is the
maximum diameter of the shell in mm.
These curves are shown in Fig. 2.
Despite a 23-fold difference in the cal-
cium content of the habitats the average
weight per square millimeter of the
shells increases only 1.2 times (10 mm
CONCHOMETRY OF BIOMPHALARIA
shells from Shiya-lo-Ngubu Dam and
Ngwetispruit). This low rate ofincrease
tends to confirmthe theory of Waddington
(1953), Warburton (1956) and others that
the development of these molluscs in
common with other organisms is con-
trolled by a cybernetic type of system,
which ensures that, within certain limits,
a phenotypically normal organism
develops despite variations in its geno-
type and developmental milieu. However,
the results for Shiya-lo-Ngubu Dam,
Outdoor Aquaria and Ngwetispruit (Fig.
2) imply that the higher calcium content
of the latter 2 habitats does tend to
give rise in the larger shells to a slight
increase in the shell weight. Boycott
(1936) found an appreciable strengthen-
ing of the shell in races of thin-shelled
Lymnaea bred in hard water. That the
concentration of calcium is not the only
factor involvedis shown by the anomalous
positions of the curves for Joubert’s
Dam and Buffelspruit and the confused
relationships between the curves at small
diameters. It is suspected from un-
published data that, in the absorbtion of
calcium by the snail, the role of other
ions is not inconsiderable and that the
concentration of these ions relative to
the calcium, especially in the case of
Joubert’s Dam, could have been respon-
sible for the slightly heavier shells from
the latter habitat. The extremely low
position of the Buffelspruit curve is not
understood. A second set of 20 shells
collected and measured more thana year
later confirmed the unusually low weight
per square millimeter for shells from
this hard-water stream. To the unaided
eye they do not appear in any way differ-
ent to shells from other habitats. Now
Buffelspruit as a habitat and also
physico-chemically is very similar and
lies almost adjacent to Boundary Creek
(Schutte & Frank, 1964). It was from
this creek that Schutte & van Eeden
(1959) reported that a certain proportion
of the shells showed an “irregularity in
the coiling of the whorls although the
rest of the shell ... was typically that
of B. pfeifferi” and they put it down to
385
ols 24 ppm Ca
MILLIGRAMS PER SQUARE MM
m
A 24 ppm Ca
y -
9
5 6 7
Я - MAXIMUM DIAMETER IN MM
FIG. 3. Relationship between shell size and
its average weight per square millimeter in
different artificial conditions.
environmental factors.
The results for the snails grown
under artifical conditions are es-
sentially similar. Unfortunately, due
to high mortality under the more un-
favourable conditions and lack of space
for more extensive cultures, only a few
snails were available, and only 10 snails
from each group were used for com-
parative calculations. In view of this
low number there seemed no justification
for calculating more than 1st degree
curves. These are shown in Fig. 3 and
were calculated as follows (у being the
average weight in mg/mm2 and a the
386
maximum diameter of the shell in mm):
:0. 0795 + 0. 00864a
0.00789 + 0.0213a
0.0789 + 0. 0289a
0.0397 + 0.0397a
ou ot
Saum
?
*The values for assumed secondary deposition, ог the reverse, were calculated according to
appendices 3 and 4 resp. Those for direct analysis are based onthe average of 3determinations.
example:
With secondary deposition:
5 = 0.0415 + 0.0157a + 0.000420a2
No secondary deposition:
y = 0.0415 + 0.0315a + 0.00126a2
They are plotted in Fig. 4.
To test whether secondary deposition
did in fact take place, the weight per
square millimeter of the shell at the
aperture was found by a more direct
method. The surface area of small
chips from the mouth of the shell was
estimated by drawing them greatly
magnified on paper with the aid of
a camera lucida. These irregularly
shaped outlines were cut out and their
weight compared with that of a piece
of known area. After dissolving the
chips in hydrochloric acid and evapor-
ating to dryness, their salts were dis-
solved in a known volume of water.
The conductivity of this solution was
then compared directly with that of a
known calcium chloride solution and
the weight per square millimeter of the
chips estimated on the assumption that
they consisted of pure calcium carbonate.
The results by this method for shells
from Shiya-lo-Ngubu Dam are also
plotted in Fig. 4. All 8 values lie below
the line given for a shell in which second-
ary deposition in the inner whorls has
been assumed to have taken place,
showing that there was no greater
average weight at the aperture, as would
be the case if growth was concentrated
there. A similar procedure wasfollowed
388 — FRANK AND MEYLING
FIG. 5. A diagrammatic cross section of portion of a shell of Biomphalaria pfeifferi showing
the various mathematical relationships discussed.
for shells from Ngwetispruit and the
Outdoor Aquaria. A comparison of the
corresponding data, for the 3 habitats,
is presented in Table 3. The figures
for the direct measurements are based
on the average of 3 samples taken from
the aperture of each shell. The values
obtained by the direct method were found
to be either below or at least nearest
the curve calculated on the assumption
that secondary deposition had taken
place. The values would have been
slightly higher if (1) allowance had been
made for the fact that approximately
4% of the weight of the shell was con-
tributed by substances other than calcium
carbonate (unpublished data) and (2) the
area in the vicinity of the sutures had
been sampled more frequently. There
was some indication that, in waters as
hard as Ngwetispruit there was a
tendency for the weight per square milli-
meter of the shell at the aperture to be
greater than the average weight per
square millimeter for the whole shell.
Five of the 7 determinations for this
habitat show values for the aperture
greater than the calculated average for
the whole shell, but still closer to the
latter than toa shell which, theoretically,
had no secondary deposition.
Shell Shape. Referring to Appendix 1,
rd = radius of whorl ur
Rg radius of spiral 1
and, from Fig. 5,
k, =sine of = РОО]
Thus should kj, supposedly a constant,
become greater, < DOOy will also be-
CONCHOMETRY OF BIOMPHALARIA
IGWETISPRUIT
0 ppm CO»
HIYA-LO-NGUBU DAM
3.7 ppm CO2
09
a 08
<
EE
m
=)
=)
+
no.
er OUTDOOR AQUARIA
2% 4.5 ppm CO»
=
06
OS
389
8 10 l2
A - MAXIMUM DIAMETER IN MM
FIG. 6. Relationship between shell size and kj (radius of whorl/radius of spiral at that point)
in different natural habitats.
come greater; or the average radius
of the whorl at the aperature relative
to the rest of the shell will increase.
Actually, since A (the rate at which the
whorls recede from the centre, Appendix
1) remains almost constant (equal to
tan a, Fig. 8, Appendix 1) the radius of
the aperture cannot easily become
greater in the plane of the spiral but
only vertical to it. Thusin any particular
Shell, while the radius of the aperture
in the plane of the spiral will be found
to be near its theoretical value, the
radii vertical to it may be greater,
giving an overall increase inthe average
radius. This condition, commonly seen
in small shells, makes the aperture
appear elliptical. The greatly in-
creased average diameter of the aper-
ture in these small shells at a con-
stant À is probably the fundamental
reason why the equation failed in
these size groups.
We may take kj therefore as an indi-
cator of any changes in the relationships
of the basic elements of the shell. The
most probable curves for kj (by least
squares) as the maximum diameter of
the shell, a, increases are, in shells
from a soft, medium and hard-water
habitat:
Shiya-lo-Ngubu Dam:
К] = 1.448 - 0.193a + 0.0098a2
Outdoor Aquaria:
К] = 1.341 - 0.198a + 0.0115a2
Ngwetispruit:
k, = 2.265 - 0.325a + 0.0145a2
390 FRANK AND MEYLING
They are plotted in Fig. 6. Withgrowth,
kı tended to change more rapidly in the
hard than it did in the softer waters,
but the differences became less as the
shells grew larger until they all had
very nearly the same value for kıata
maximum shell diameter of about 9mm.
The relatively greater values found for
k] in small shells from Ngwetispruit (the
difference disappeared as the shells grew
larger) may be taken to indicate that not
only was the aperture more elliptical in
these hardwater snails but that the
whorls must have overlapped more, for,
the larger К] is, the greater will be the
overlap of one whorl over the preceeding
one. As Huxley (1932) points out, this
lends greater strength tothe shell. Since
for a given perimeter (in this case shell
wall) a circle circumscribes a greater
area than an ellipse, and since the less
overlap there is, the less the earlier
whorls protrude into the later whorls,
a small soft-water shell will have a
greater internal volume and can thus
contain a larger snail than a hard-water
shell of the same average radius of
aperture. Put another way: in early
life soft-water snails with their more
nearly circular shell whorls and less
compact structure tend to use their
calcium carbonate more “economically”
than their hard-water counterparts. This
implies that in a given time, hard-water
snails, if their soft-parts are to occupy
the same volume, must produce a greater
number of whorls than their soft-water
counterparts of equivalent age.
If water-hardness (Table 1) alone is
taken into consideration as a factor
influencing shell “shape” (a decrease in
К] denoting greater relative flattening)
then it would be expected that the curve
(Fig. 6) for Outdoor Aquaria (37 ppm
CaCO3) should lie between the other
two (Ngwetispruit: 114 ppm; Shiya-
lo-Ngubu: 5ppm). However, ifaggressive
carbon dioxide should be the overriding
factor for control it will be seen thatthe
curves lieinalogical sequence, Ngwetis-
pruit with the lowest value for aggressive
carbon dioxide (0 ppm) having the highest
values for ky in any size group and
Outdoor Aquaria with the highest value
for carbon dioxide (4.5 ppm) having the
lowest values for k, in equivalent size
groups. Furthermore, the results for
artifical media, would on the whole, seem
to confirm this suggestion, the least
aggressive condition having the greatest
values for kj in equivalent size groups.
The most probable curves (again lst
degree in view of the small number of
Shells) are plotted in Fig. 7 and are
calculated as follows:
А: k, = 0.755 - 0.0367a
В: kj = 0.669 - 0.0258a
С: К, = 0.868 - 0.0526a
D: К; = 0.800 - 0. 0533а
However, the fact that the values for kj
in shells from the hardest artifical
medium (D, 98 ppm CaCO3) do not fit
this scheme, and, as mentioned before,
that anomalies exist in the weight/mm2
relationships of shells from Buffelspruit
and Joubert's Dam, give reason to
suspect that there are factors, other
than the concentration of calcium and
carbon dioxide, which affect shell growth
and shape, especially where the concen-
tration of calcium relative to the other
ions in solution is disproportionate.
DISCUSSION
It is unfortunate that the collections
used in the present study were not ob-
tained from exactly the same sites as
those of Schutte € van Eeden (1959) in
their work on the shell of Biomphalaria
pfeifferi. It is also regretted that no
physico-chemical data are available
from their collecting sites. Neverthe-
less, it is thought that the habitat con-
ditions were sufficiently similar in the
2 studies for a useful comparison of the
2 methods of attack and their results to
be made.
(a) Our work has confirmed Schutte
and van Eeden’s suggestion that only
equivalent size groups should be com-
pared and not mean values from
CONCHOMETRY OF BIOMPHALARIA 391
O6
0.55
D 2.9 ppm COz
SHELL SHAPE
А, -
о
ua
5 6
B 8.4 ppm СО2
7 8
а MAXIMUM DIAMETER IN MM
FIG. 7. Relationship between shell size and kı (radius of whorl/radius of spiral at that point)
under different artificial conditions.
measurements of random samples,
since, in our case, kj (radius of aperture
to that of the spiral) and in theirs the
related, though inverse ratio D/H
(greatest shell diameter to shell height)
changes as the shell grows larger.
(b) The marked convergence of values
for К] or “shape” (Figs. 6 and 7) and to
a lesser extent for Y or average weight/
mm? (Fig. 2) for shells between 8 and 9
mm in diameter is paralleled in Schutte
and van Eeden’s results. Their related
D/H ratios for samples from various
habitats, also differ more from one
another in the greater (10-12 mm) than
in the smaller (8-10 mm) groups. Un-
fortunately they list only 2 samples in
the 6-8 mm size group, but both of these
have (statistically) highly significant
differences. They also state in general
for their material and ratios that
“samples usually differ more from one
another in the greater thaninthe smaller
size groups”.
(c) Using ground cross-sections of
Shells Schutte and van Eeden measured
the greatest distance (their “major dia-
meter”) across each whorl. This “major
diameter” usually lies approximately at
right angles to the plane of the spiral
(see their Fig. 5). Our data suggest
that (1) because kj is not constant (Fig.
6) the relative size of the aperture proba-
bly varies, but that near a maximum
shell diameter of 9 mm the change
becomes slight and is similar for snails
from different localities and that (2) the
whorl radii, vertical to the plane of the
392 — FRANK AND MEYLING
spiral, are exaggerated in the earlier
parts of the shell. Schutte and van
Eeden's figures also show that over
the range 8.5-10.5 mm the ratios the
“major diameter” of the penultimate
to ultimate and the pre-penultimate to
penultimate whorls were constant, but
that the ratio for the inner whorls was
higher than for the outer. The present
work suggests, however, that the outer
whorls have the greater ratio. The
discrepancy is probably due to the fact
that our conclusions were based on an
average diameter whereas theirs were
based on the “major diameter”. Al-
though the ratio of the ultimate to pen-
ultimate whorls is virtually constant over
the range 8-10 mm, Schutte and van
Eeden contradict their figures by saying
that these ratios do not vary with the
age of the shell.
(d) It is clear from Figs. 6 and 7 that
К] varies a great deal during the life of
the snail and that its rate of change for
specimens from different habitats is
different. The data further suggest
that the alteration in the rate of change
in К] is brought about not by the calcium
but by the aggressive carbon dioxide of
the water. Thus it is very doubtful
whether either k (the radius of the
whorl relative to the radius of the spiral
at that point) or the measurement of
shell angles (Schutte & van Eeden, 1959,
Fig. 5, = EQF and
Calculation of Н$
From Fig. 1 and Appendix 1
Il
p
Rp + kiRÿ + Rór + k¡Ró-7r
Вф + гф + Вф-т + тф-т
ll
p
Ro + Rór = —*—
1-k
R pr
But as Dem = AO IN = RN AN
R-7 Ce®- TÍA e-TA
Вф-т = Re ™ or according
to (7)
Rg [ka and substituting
in the above
equation
a
Rg (1 + fk,) = Я
er, a
Te Ky) (1 + Jk) AN
Calculation of k;
T
or according to (8)
bis ky
ua AA)
Calculation of Bo
From Fig. 5
rg = h2 + x?
"hon =h* + (y-x)2
rg - та = x2- y2 + 2yx - x2
= 2yx-y 2
But “y = Rg - R-27
r$- $27 = 2(Rg- Rg_o7)X - Rg - Rp- 2m)?
$ Thon) + Rp- Rp-2m2
2Rg-Rg am)
De
CosBo = 1
i
_ gran * Rp Вот
2rp(Rá - Вф-2т)
According to (6) and (1)
Eb k¡Rg:
Rg oy =KoRps tp9,=kyRo-27=k1XkgxRo
„RO? - Слов? + Rp-kong)?
a Gé TES)
kı(l + k 1-k
ee es i
2 2k,
398
FRANK AND MEYLING
APPENDIX 4 meter at the aperture of a shell
in which no secondary depo-
The equation for the weight per unit sition occurs.
area of the shell at the aperture
when no secondary deposition
takes place or substituting values for shells from
Let y
and y
then [yaa = ay
Shiya-lo-Ngubu Dam
= shell weight per square milli-
meter at the aperture of a shell
in which secondary deposition and differentiating to a
occurs (same as the average
к уда = (0. 04154а + 0.01573 x 2ada +
weight/sq mm).
= shell weight per square milli- у = 0.0415 + 0.03146a + 0. 0012594a2
RESUMEN
CONTRIBUCION A LA CONCHOMETRIA DE BIOMPHALARIA PFEIFFERI
(BASOMMATOPHORA: PLANORBIDAE)
En comün con muchos moluscos, la concha de Biomphalaria pfeifferi forma una
espiral logaritmica. La forma real de esta espiral es cercana a la ideal. Ecuaciones
basadas en este aspecto, se usaron para calcular el ärea superficial y su peso por
mm2. Como control, se hicieron estimaciones por un metodo mas directo, encon-
trandose substancial concordancia. Resultados tomados de conchas de ambientes
naturales y artificiales, sugieren que el peso medio por mm2, crece con la edad y
el aumento del calcio soluble en el medio ambiente. Este crecimiento tiene lugar,
aparentemente, en todas las partes de la concha por ejemplo, el peso por mm2 de una
parte es aproximadamente igual a la medida media de la concha entera. Pareceria
que el valor Ky(radio del anfracto/radio de la espiral a ese punto) o su proporciön
equivalente, altura a diametro maximo, decrece con la edad y con el aumento del
agresivo carbon diöxido del habitat. Si, como el resultado de esta limitada investi-
gación sugiere, la concha de Biomphalaria siempre se aproxima a la forma ideal,
conchometría detallada por métodos convencionales es innecesaria. Análisis mate-
mático completo se requerirá solo si se encuentra que la valuación (A) de recesión
de las vueltas desde el centro y el diametro de la abertura (relacionado con rg) en
grupos de tamaño similar, es significativamente diferente.
| уда = а(0. 0415 + 0.015734a + 0. 0004198a2)
0. 0004198 x 3a2da)
MALACOLOGIA, 1966, 3(3): 399-418
THE GENUS MYA IN THE ARCTIC REGION
Dan Laursen
Department of Biology and Earth Science
Jackson County Community College
Jackson, Michigan, U. 5. A.
ABSTRACT
The present account was written to clarify a misconception about Arctic spe-
cies of Mya. Jensen (1900) has pointed out (in Danish) that all the then existing
records of М. arenaria Linnaeus from the Arctic were erroneous and dealt, in
fact, with a form of M. truncata Linnaeus which he named ovata. The most re-
liable distinguishing marks between the almost similar shells of the 2 species
lie in the cartilage plate of the left valve and the corresponding cartilage pit of
the right valve. However, because Jensen’s publication is not widely known in
the English speaking world, М. arenaria, a boreal species, is still being re-
ported from the Arctic. Furthermore, Schlesch (1931) arbitrarily elevated the
form ovata, which Jensen himself considered at most to be an infrasubspecies,
to species rank, and renamed it M. pseudoarenaria, a name that should not be
used.
In this paper, the distribution, Recent and fossil, of 3 forms of Mya truncata:
M. truncata forma typica Linnaeus, M. truncata f. uddevallensis Forbes andM.
truncata f. ovata Jensen, as well as that of M. arenaria is given, as far as it
could be ascertained. The lists are not complete. Scientists working with M.
truncata are entreated to give more details regarding forms in future papers.
Some new records of M.arenaria from within the Arctic regions are dis-
INTRODUCTION
In 1900, Adolf S. Jensen, the now
deceased Professor Zoologiae at the
University of Copenhagen, published a
paper entitled: “Studier over nordiske
Mollusker. I. Mya.” (Studies of Nordic
Molluses. I. Mya.), in which he demon-
strated that all the specimens from the
Arctic Region collected prior to 1900
and identified as Mya arenaria Linnaeus
are a variety of Mya truncata, which he
named ovata. The paper was written
in Danish and, unfortunately, very few
malacologists outside of Scandinavian
countries benefited from it. H.Schlesch
(1931) treated the topic in German.
Jensen was occasionally quoted in the
English language malacological liter-
ature and recently Foster (1946) treated
the genus and the problems associated
with it in his paper dealing with Mya in
cussed, all of which deal with M. truncata f. ovata.
the Western Atlantic. Every now and
then, however, the old confusion and
misconception about the Arctic species of
Mya turns up again in papers written
in the English speaking parts of the
World, even though Jensen clarified the
issue more than 60 years ago. This
paper is an attempt to prevent the
perpetuation of this error.
There follows a summary of Jensen’s
(1900) paper supplemented by some later
information, a revision of more recent
records, distribution lists and a dis-
cussion.
JENSEN’S CONTRIBUTION
The melting of the Great European
Ice Cap caused an immediate sub-
mergence of low level areas in southern
Scandinavia. Further deglaciation, how-
ever, caused an isostatic uplift of the
(399)
400 D. LAURSEN
same area whereby the original Baltic
basin was turned intothe Baltic Ice Lake,
a freshwater lake fed by the meltwater
from the still existing ice and drained
through the straits and sounds now con-
necting the Baltic Sea and the North Sea.
Because of a new depression of the
earth’s crust, salt water entered the
Baltic basin, forming the Yoldia Sea,
which is named for its dominant inhabit-
ant, the high-arctic bivalve Yoldia
arctica Gray (=Portlandia arctica
(Gray)). A new uplift again raised the
Baltic area, and the sea was converted
into a freshwater lake, the Ancylus Lake,
named after its characteristic species
Ancylus fluviatilis Müller.
The steady eustatic rise of sea level
caused by the still melting ice again
gradually submerged the basin with its
associated sounds and belts. The An-
cylus Lake became part of the water
body called the Littorina Sea (named for
the gastropod Littorina littorea Linn-
aeus). This lake finally became the
present Baltic Sea.
During the last quarter of the 19th
century the post-glacial deposits of
northern Europe were studied in-
tensively. Little by little the migration
patterns of the present inhabitants of
the North Sea and the Baltic Sea were
revealed. One fact, however, puzzled
interested scientists. Mya arenaria,
which now occurs regularly along the
coasts of Denmark and southern Sweden,
did not occur at all as a fossil in the
layers investigated. Nathorst (1872)
was the first to direct attention to this
fact and it was later confirmed by
Petersen (1892). In the older deposits
Petersen found several genera (Tapes
and Ostrea) which do not occur in the
area today. The Tapes deposits are
contemporary with extensive kitchen
middens where Mya arenaria is absent.
It must have immigrated later. This is
also the situation in northwest Germany
(Berendt, 1867; Mendthal, 1889), in Got-
land and Oland in Sweden (Lindström,
1868), in Norway (M. Sars, 1865) andin
Belgium (Raeymaekers, 1895).
The question which then arose was:
where did Mya arenaria live before its
immigration to these regions and from
where did it emigrate? The answer
seemed very easy. From the available
distribution records of this species it
had to be: from the north. All con-
temporary authors dealing with the dis-
tribution agreed in classifying M. aren-
aria as an Arctic, circumpolar species
occurring in Labrador, Greenland, Spits-
bergen, the Kara Sea, along the Siberian
coast and in the Bering Strait. At the
same time, however, aninvestigation of
the distribution during the Glacial Period
showed the species to be absent from
Denmark (Johnstrup, 1882; Jessen,
1899) and the Scandinavian peninsula (M.
Sars, 1865; Thudén, 1886).
This appeared contradictory to Jensen.
He felt that a species now living through-
out the entire Arctic zone would certainly
have lived in northern waters with the
arctic climate prevailed during the
Glacial Period. He began an investi-
gation of the problem and proved that
the classification of Mya arenaria asa
high-arctic species was due to a wide-
spread misconception. He examined
every specimen mentioned in the liter-
ature and an overwhelming amount of
material available in museums and
private collections, and was able to
demonstrate that all statements about
the presence of M. arenaria in high-
arctic regions were due to misidentifi-
cation.
Jensen gave a detailed account of the
differences between Mya arenaria and
M. truncata that are useful for identifica-
tion. The most reliable distinguishing
marks are found in the chondrophores of
the left and right valves: the cartilage
plate of the left valve and the corres-
ponding cartilage pit of the right valve.
He also mentioned the diagnostic im-
portance of the umbones of the left
valve. For a complete, detailed
description see Foster (1946).
Jensen used these characteristics ina
revision of the high-arctic specimens
earlier identified as Mya arenaria, which
ARCTIC MYA
he recognized as a special form of M.
truncata that he named forma ovata. He
then critically evaluated all literature
records of “M. arenaria” from the high-
arctic regions. The specimens from
Greenland reported by Fabricius (1780),
Möller (1842), Mórch (1857), Posselt
(1898), Traustedt (1883), Nordenskiöld
(1870) and Bay (1895) were all found to
be M. truncata forma ovata, andaccord-
ingly M. arenaria must be withdrawn
from the list of Recent and fossil bi-
valves of that island. The same applies
to the records of M. arenaria from Ice-
land (Mohr, 1786; Mprch, 1868 and
Posselt, 1898); from Spitsbergen
(Kröyer (unpublished; see Jensen;
specimens in the Zoological Museum,
Copenhagen); Meyer & Möbius, 1872;
Friele,1879); from the KaraSea (Leche,
1883; Collin, 1886); and from the
Siberian Sea (Leche, 1878).
The occurrence of Mya arenaria in
Labrador, both Recent and fossil is
mentioned by Packard (1867). A
collection of American shells, donated
by Packard, is in the Zoological Museum
in Copenhagen. Some shells from the
Pleistocene of Maine, identified by
Packard as M.arenaria are actually
M. truncata forma ovata, and no doubt
some of the specimens cited by Packard
elsewhere are also forma ovata. Packard
also sent shells from Maine, the Mari-
time Provinces and Labrador to the
University Museum, Oslo, Norway.
Brégger (1900/01) gives the information,
that the specimens from the southern-
most locality, identified by Packard as
M. arenaria, are true M. arenaria, but
those from the northern localities are
partly M. arenaria and partly M. trun-
cata forma ovata. Otherwise Вгфосег
agrees with Jensen’s interpretation of
the American shell material.
Krause (1885) has stated that very
young Mya arenaria are present in the
Bering Strait. Jensen demonstrates
that in many instances such young speci-
mens of M. truncata are misidentified,
as they have not yet developed the trun-
cate posterior end. The Bering Strait’s
401
specimens are similar and all records
of M. arenaria from this locality must
be considered erroneous.
Jensen finally gave the distributions
of the species as known at the turn of
the century. Their presently known
distributions will be given below.
NEW REVISIONS AND RECORDS
Baker (1911), Wilson (1904) and Mc-
Innes (1904) record Mya arenaria from
the Pleistocene of James Bay, Canada.
Richards (1936), who later investigated
the same area, did not find M. arenaria
in the deposits. Probably the 3 first
mentioned scientists were influenced by
the old idea that M. arenaria was an
Arctic species and had no knowledge of
Jensen’s paper.
It was possible to find the shell col-
lected by McInnes at Winisk River. It
is an unbroken left valve with an al-
most rounded but still recognizable trun-
cate posterior end. It has a chondro-
phore of the truncata type and also the
pallial sinus is truncata-like. The shell
must therefore be identified as Mya
truncata (Canadian Geological Survey
cat. no. 66355).
Nichols (1936a), while with the Eastern
Arctic Expedition during 1935, collected
Shells from the raised terraces in the
Hudson Bay area. The shells were
identified by A. LaRocque. Mya arenaria
is recorded from the following localities:
Sugluk, Quebec, Elevation 224 ft.
Port Harrison, Quebec. Elevation 110
at.
Port Harrison, Quebec. Locality 2.
Elevation 20-42 ft.
Port Harrison, Quebec, Elevation
124 ft.
Port Harrison, Quebec. About 1 mile
south. Elevation 162 ft.
Shells were also collected at Eric
Cove, Wolstenholme, Quebec. Elevations
233 and 345 ft.
From the Geological Survey of Canada,
I received some samples of Mya shells
in addition to the one collected by
McInnes. These samples are listed and
402 D. LAURSEN
discussed below.
Sample 1.
Locality: Clyde River, Baffin Island. Alt.:
40-180ft (13.3-60m). Collected by: D.
A. Nichols, 1937. Canadian Geol. Surv.
cat. no. 66353,
The sample consists of 1 large, un-
broken left valve, 1 large and 1 small
unbroken right valve, plus several frag-
ments, some of them with chondrophore
and/or-pallial sinus.
Mya truncata forma ovata. Two large
shells. For the dimensions of these
shells and the following see Table 1.
Mya truncata forma typica. One
small shell and several fragments.
Sample 2.
Locality: Port Harrison, Quebec. Col-
lected by: D. A. Nichols. Canadian
Geol. Surv. cat. no. 66352.
The sample consists of 4 unbroken
Shells: 2 large left and 1 small left
valve, and 1 large right valve plus a
fragment. Allthe shells are Mya trun-
cata forma ovata.
Sample 3.
Locality: Eric Cove, Quebec. Alt.:
12-32 ft (4-11m). Collected by: D. A.
Nichols, 1936(?).
cat. no. 66354.
The sample consists of 1 whole speci-
men, 4 unbroken valves, and several
large fragments, most of them with
chondrophore.
Mya truncata forma typica. One speci-
men, 2 unbroken right valves and several
fragments.
Mya truncata forma ovata. Two valves,
a left one and a right one.
Sample 4.
Mya arenaria ?
Locality: Fort Albany, Ontario. North
side of Albany River in clay beds. Col-
lected by: Fritz Johansen, July 8, 1920.
Canadian Geol. Surv. cat. no. 66351.
The sample consists of 1 unbroken
shell and a large fragment.
Mya truncata forma typica. One
large fragment.
Mya truncata forma ovata.
valve.
As can be seen from the above, the
Canadian Geol. Surv.
One left
old identification of Mya arenaria at
Port Harrison is not correct. The
sample I have checked has no record
of elevation, but if M. truncata forma
ovata was misidentified from one ele-
vation, I think this would also happen
to the forma ovata shells from the other
elevations. For the same reason I also
believe that the Mya specimens from
Sugluk and Wakeham Bay identified as M.
arenaria really are М. truncata forma
ovata Jensen. Strangely enough, the
only Mya specimens recorded from Eric
Cove are all M. truncata forma uddeval-
lensis Forbes, whereas forma typicaand
forma ovata, present in the sample I got,
are not recorded at all by Nichols
(1936a,b). However, the sample might
be from 1937 and therefore not included
in the report.
Richards (1940b), records 1 specimen
of Mya arenaria from the west coast of
Hudson Bay near the north side of Dawson
Inlet, about 60 miles north of Eskimo
Point. Upon my request Dr. Richards
was kind enough to reexamine the speci-
men. He informed me that upon further
examination he finds it such a young
specimen that it should be identified
merely as Mya sp.
Since all traceable specimens of Mya
avenaria recorded from the Hudson Bay
area turned out to be M. truncata forma
ovata, M. arenaria must be omitted from
the faunal lists of that region.
Elton & Baden-Powell (1931) record
the presence of M. arenaria in raised
beaches from Spitsbergen. Feyling-
Hanssen & Jgrstad (1950) point out the
mistake and identify the specimen found
as M. truncata forma ovata.
In a paper by Davies, Krinsley &
Nicol (1963, p 51-52), it is stated that
Mya arenaria was collected on the beach
at Narssarssuk, about 20 km southwest
of Dundas Airbase, Thule District, North
Greenland. It is not indicated whether
the shells are Recent or subfossil. They
are compared with shells collectedfrom
raised beaches, which may indicate that
the authors consider the shells from the
present beach as Recent. However, M.
ARCTIC MYA
arenaria does not live and presumably
never did live in Greenland waters. The
shells were identified by Dr. Harald A.
Rehder, Smithsonian Institution. I asked
Dr. Rehder to reexamine the specimens
but unfortunately they were thrown away,
and there is no other record of the
identification than the one in the above
cited paper. Dr. Rehder has therefore
stated that he regards the record of
Mya arenaria from the Thule District
as a doubtful one. I consider that the
record of M. arenaria in the faunal list
of Davies et al. is incorrect. If the
shells were found in North Star Bay,
the harbor of Dundas Airbase, it is
just possible that the species could have
been transported from a warmer latitude.
However, even if the number of ships
calling at North Star Bay were greatly
increased, the chances for such transport
seem to me extremely remote, especially
when considering the normal habitat of
Mya arenaria. A subsequent migration
of the species from the bay to Nars-
sarssuk is unthinkable under the circum-
stances.
It seems to me that there is no doubt
about the specimens from Thule being
either very young Mya truncata forma
typica or M. truncata forma ovata. The
temperature of the water in North Star
Bay and Wolstenholme Sound is much too
low for M. arenaria, being about 20C at
the surface in August and 1%C at 10m
depth (Riis-Carstensen, 1936). Gener-
ally, the species occurs in shallow water
(0-6 m), occasionally to a depth of 25 m.
The average temperature for the coldest
month (February) of the northern locali -
ties where true Mya arenaria is recor-
ded, ranges from about 0°C (Okhotsk Sea)
(Krümmel, 1911) to 6°C (southern Nor-
way) (Helland-Hansen & Nansen, 1909).
For the southern localities, the average
temperature of the coldest month ranges
from about 10-110C (France, Japan) to
about 15°C (Cape Hatteras). The average
temperature for the warmest month
(August) ranges from about 5°C
(Labrador) to about 10-119C (Akutan
Island, Kamchatka, northern Norway).
403
The temperature for the warmest month
in the southern localities ranges from
about 15°C (California) and 21°C (south-
ern France) to about 25°C (Cape
Hatteras, Japan). The temperatures
above are taken from: Sverdrup,
Johnson & Fleming (1961); publications
of The Hydrographic Office, Washington
D. C.; Department of Transport, Ottawa;
Det danske Meteorologiske Institut,
Copenhagen; Norsk Polarinstitut, Oslo
and Seewarte, Hamburg.
Spawning of Mya arenaria takes place
in May-June off Japan (Yoshida, 1938),
and in June in Danish waters (Barker-
Jórgensen, 1946) and off Labrador
(Stafford, 1912). The larvae of M.
truncata occurred in Danish waters from
October to March with a maximum
occurrence in November-January (Bar-
ker-Jörgensen, 1946). In northeast
Greenland Thorson (1936) found M. trun-
cata spawning from June to September,
reaching amaximumin July. The surface
temperature of the Danish waters during
the season the veliger of M. truncata is
abundant is about 5°C —the same temper-
ature found in east Greenland waters
when M. truncata veligers are abundant
(Spärck, 1933).
It seems as if Mya arenaria in its
veliger stage needs a temperature of
about 12-15°C, and that Labrador is an
exception. A calculation based upon
available temperatures in the reports
from the various institutions mentioned
above, from 1946-1956, gives tempera-
tures’ of 5°C, 79C’ and 6°C ‘for July,
August and September (respectively) in
the area supposed to be the northern
limit of M. arenaria. However, the
temperatures are taken outside the area
where M. arenaria generally is found.
In the actual area the surface tempera-
ture may be a few degrees higher. The
lowest observed surface summer
temperature off Nain, Labrador, was
about 30°C (July 1952) and the highest
11.70C (August 1954). Besides, these
temperatures were obtained in navi-
gable water. No doubt there are years
with a temperature high enough for
404 D. LAURSEN
TABLE 1. Dimensions of Mya shells, revised or newly-recorded, from Canada
Locality
Winisk River,
James Bay
Clyde River
Alt. 40’-180°,
Baffin Island
22
Port Harrison,
Quebec
Eric Cove, Quebec
left shell
right shell
Mya truncata forma typica
DEN:
Mya truncata forma ovata
62
Fort Albany,
Ontario
+ :
д Height x 100
Index renee
veligers to survive.
Unfortunately we do not know as much
as we would like about Mya arenaria
on the Canadian coast. М. arenaria,
a boreal species, must be considered a
key species. Its presence as a Pleisto-
cene fossil in the coastal areas of Hudson
Bay would give valid proof of a warmer
period during part of the Pleistocene,
than that which presently exists. An
indication of such a warmer period in
Canada, as demonstrated earlier in
Greenland (Jensen & Harder, 1910;
Harder et al., 1949), is givenby Laursen
(1946 p 43-46), but more convincing
proof is needed, such as actual demon-
stration of the presence of Mya aren-
aria in raised beaches north of its
present northern occurrence.
DISTRIBUTION
Soot-Ryen (1932), in a paper on the
Norwegian “Maud” Expedition, uses the
term “true circumarctic” to designate
speciesthat arefound continuously along
the coasts of the Arctic Ocean and
“circumarctic” for those only occurring
sporadically along the coast. The old
term “circumpolar” is, according to
Soot-Ryen, used for species occurring
in the northern Pacific and the northern
Atlantic, even if they are missing on
the arctic coasts of Eurasia and
America. As a temporary aid, the
terms proposed by Soot-Ryen are used
here.
In most papers where Mya truncata
is mentioned, no sharp distinction is
made between forma typica, forma ud-
devallensis and forma ovata. This may
be adequate when dealing with small
areas, but where the coasts of large
regions or even continents are involved
it is insufficient. Papers available to
the present author too often give insuf-
ficient information as to the presence or
absence of the 2 extreme forms. In
the following discussion, vague infor-
mation has been disregarded.
The fact that animals are not recorded
from a specific area, does not mean
ARCTIC MYA 405
FIG. 1. Geographical distribution of Mya truncata forma typica Linnaeus.
O = living
O = fossil
The signs only in-
dicate the geographical unit (sea, island group, region, etc.) from where the speci-
mens are recorded.
that they are absent. On expeditions in
the arctic seas, scientists very often
are obliged to use ahand bottom sampler
and hand dredge, which are ineffective
in collecting deep-burrowing species
such as those of the genus Mya. Intro-
duction of new gear, and especially
heavier gear, can give better results than
have been. obtained earlier (see also
Soot-Ryen, 1951).
It is often very difficult to determine
if a species really lives in the area
from where the shells are recorded. In
many regions the shells may originate
from extensive submerged Pleistocene
shell banks. If there is no indication
406 D. LAURSEN
whether the collected specimens were
entire animals or only empty shells, a
decision is difficult. And even when
information is on record it may be
incorrect because recent shells may
look very old, due to corrosion, where-
as subfossil (Pleistocene) shells often
look very fresh indeed.
To give a complete list of all records
of both recent and fossil Mya arenaria
and M. truncata shells is a time-con-
Suming project. At the time Jensen
made his studies, more than 350 papers
would have had to be examined just to
give the Recent distribution, and at
least another 200 for the fossil shells.
During the more than 60 intervening
years, several thousand papers dealing
with the Mya family have been published.
Moreover, scores of museums all over
the world have collections about which
nothing has been published.
The following indications of distri-
bution are therefore far from precise
or complete and perhaps the attempt
should not have been made. The present
object is, however, to encourage zoolo-
gists, geologists and malacologists to
give as much information as possible
in future papers in which Mya arenaria
and M. truncata are discussed.
Recent Distribution
Mya truncata forma typica
Linnaeus (Fig. 1)
(True circumarctic)
North Greenland: Port Foulke (Jeffreys,
1880); West Greenland (Fabricius, 1780);
East Greenland: Jórgen Brónlund Fjord-
Qegertatsiaq (Ockelmann, 1958); Jan
Mayen (Becher, 1886); Spitsbergen
(Torrell, 1859); Franz Joseph Land
(Cattie, 1886); Novaya Zemlya (Leche,
1878); Barents Sea (Norman, 1881);
Norwegian Finmark (Sars, 1878); Mur-
man Coast, Murman Sea (Middendorff,
1849); White Sea (Leche, 1883); Kara
Sea (Leche, 1883); Laptev Sea (Leche,
1883); East Siberian Sea (Middendorff,
1851); Chukchee Sea (Middendorff, 1851);
Bering Strait, BeringSea (Krause, 1885);
Kamchatka Peninsula (Middendorff,
1851); Sea of Okhotsk (Middendorff,
1851); Kuril Island (Lamy, 1926); Hako-
dadi, Japan (Lamy, 1926); Alaska (Dall,
1924); British Columbia; Port Orchard,
Puget Sound, Washington (Foster, 1946);
Beaufort Sea (Hägg, 1904); Canadian
Arctic Archipelago (Hägg, 1904); Labra-
dor, Newfoundland, Massachusetts: Nan-
tucket (Foster, 1946). Iceland (Öskars-
son, 1952); Faroe Islands (Posselt,
1898); Between Jan Mayen and northern
Norway (Sars, 1878); Norway (Sars,
1878); southwestern Sweden (Hägg,
1904); Denmark (Petersen, 1888); Baltic
Sea, western part (Meyer & Möbius,
1872); North Sea (Jeffreys, 1865);
British Isles (Jeffreys, 1865); Germany
(Jaeckel, 1952); Netherlands, Belgium,
France south to La Rochelle (Dautzen-
berg, 1913); Rockall (a rock in the
Atlantic west of Scotland) [dead shells]
(Johansen, 1902).
Mya truncata forma ovata Jensen
(Fig. 2)
(Circumarctic)
West Greenland (Jensen, 1900); East
Greenland (Jensen, 1900); Iceland
(Jensen, 1900); Spitsbergen (Jensen,
1900); Franz Joseph Land (Feyling-
Hanssen, 1955); Novaya Zemlya (Jensen,
1900); Kara Sea (Jensen, 1900); Bering
Sea (Jensen, 1900); Sea of Okhotsk
(Middendorff, 1849); Alaska (Midden-
dorff, 1849); Labrador (@yen, 1915);
Newfoundland (Whiteaves, 1901).
Mya truncata forma uddevallensis
Forbes (Fig. 3)
(Circumarctic ?)
North Greenland: Port Foulke (Jeffreys,
1880); West Greenland (Posselt, 1898);
East Greenland (Jenser, 1905); Jan
Mayen (Hägg, 1904); Iceland (Torrell,
1859); Spitsbergen (Hägg, 1904); Franz
Joseph Land (Hägg, 1904); Novaya Zem-
lya (Sars, 1878); Barents Sea (Sars,
1878); Ponds Inlet (Laursen, 1946);
Baffin Island (Hägg, 1904); Hudson Strait
(Hägg, 1904); Labrador (Hägg, 1904);
Gulf of St. Lawrence (Forbes, 1846);
ARCTIC MYA
407
O = living
@ = fossil
FIG. 2. Geographical distribution of Mya truncata forma ovata Jensen.
Norway (Sars, 1878).
Mya arenaria Linnaeus
(Fig. 4)
Eastern Atlantic: West Coast of Nor-
way (Sars, 1878); southern Sweden,
Denmark (Petersen, 1888); the Balticto
62036' N. Lat. (Petersen, 1888); west
coast of Germany (Jaeckel, 1952); the
Netherlands, Belgium (Raeymaekers,
1895); France to the Bay of Biscay
south to Arcachon (Dautzenberg, 1913).
Western Atlantic: Nain, Labrador to
Virginia Beach and Chesapeake Bay
(Foster, 1946). Dead valves recorded
from Beaufort, North Carolina (Foster,
1946).
Eastern Pacific: Akutan Island,
Alaska; Puget Sound, Washington; Mon-
terey, California (Foster, 194%)
408 D. LAURSEN
O = living
O = fossill
FIG. 3. Geographical distribution of Mya truncata forma uddevallensis Forbes.
Western Pacific: From the southern
part of Kamchatka Peninsula and the
Sea of Okhotsk and across the Tartar
Strait to the mainland and south to
Nagasaki, the east coast of Sakhalin
included (Lamy, 1926); east coast of
China (Yent’ai) (Crosse & Debeaux,
1863).
Fossil Distribution
Mya truncata forma typica
Linnaeus (Fig. 1)
West Greenland (Posselt, 1898); East
Greenland (Jensen, 1905); North Green-
land (Jensen, 1917); Jan Mayen, Iceland
(Thoroddsen, 1892); Spitsbergen (Fey-
ARCTIC MYA 409
O = living
@ = fossil
FIG. 4. Geographical distribution of Mya arenaria Linnaeus.
ling-Hanssen, 1955); Novaya Zemlya
(Knipowitsch, 1900); Murman Coast and
the north coast of Siberia as far east
as Cape Chelyuskin (Grgnlie, 1928), San
Pedro, California (Clark, 1931). North-
west Territory, Canada (Washburn,
1947); Victoria Island (Washburn, 1947);
Baffin Island (author); Hudson Bay,
James Bay, Labrador, Newfoundland,
Rivière du Loup, Montreal and St.
Lawrence Valley, New Brunswick, Main
(Richards, 1940a,b). Dredged off Bear
Island and Rockall (Johansen, 1902);
Norway (Brögger, 1900/01); southwest
coast of Sweden (Hessland, 1943); Den-
mark (Nordmann & Madsen, 1928); Ice-
land (Thoroddson, 1892); The Nether-
lands (Nordmann, 1928); Scotland
410 D. LAURSEN
(Munthe, 1897).
Pliocene: Iceland, England (Schlesch,
1924). |
Mya truncata forma ovata Jensen
(Fig. 2)
West Greenland (Jensen, 1900); East
Greenland (Jensen, 1905); Iceland (Jen-
sen, 1900); Spitsbergen (Jensen, 1900);
Franz Joseph Land (Feyling-Hanssen,
1955); - Novaya Zemlya (Jensen, 1900);
Mouth of Yenisey River, Siberia
(Schmidt, 1872). Canada: Vansittart Is-
land (Laursen, 1946); Northwest Territo-
ries (Craig & Fyles, 1960; Craig, 1961);
Port Harrison, Quebec; Eric Cove, Que-
bec; Fort Albany, Ontario (author); La-
brador (Jensen, 1900); Maine (Brógger,
1900/10). Norway (Soot-Ryen, 1951).
Pliocene: Iceland (Schlesch, 1924).
Mya truncata forma uddevallensis
Forbes (Fig. 3)
West Greenland (Laursen, 1944); East
Greenland (Laursen, 1954); Iceland (Bar-
darson, 1921); Norway (Brögger 1900/
01); southwestern Sweden (Hessland,
1943); Denmark (Petersen, 1888); Spits-
bergen (Feyling-Hanssen, 1955); Mouth
of Yenisey River (Schmidt, 1872). Cana-
da: Kuwatin, northern district, Northwest
Territories (Craig, 1961); Baffin Island,
southern part (Nichols, 1936b); northern
part (Laursen, 1946); Vansittart Island
(Laursen, 1946); White Island (Laursen,
1946); Sugluk, Quebec (Nichols, 1936b);
Port Harrison, Quebec (Nichols, 1936b);
Churchill, Manitoba (Nichols, 1936b).
Mya arenaria Linnaeus
(Fig. 4)
North America: St. Lawrence Valley,
Champlain Valley, Massachusetts to New
Jersey (Richards, 1940a,b).
Europe: Pliocene: Red Crag and
Norwich Crag, England (Schlesch, 1924).
DISCUSSION
Jensen’s paper did not cause contro-
versy within the contemporary mala-
cological world, as his arguments were
generally accepted. Not until 30 years
later did the discussion start.
Schlesch (1931: 136-137) considered
Mya truncata forma ovata a valid species
and renamed it M. pseudoarenaria.
Schlesch, however, does not support his
decision with evidence, nor does he in-
form us why he recognizes M. truncata
forma ovata Jensen as a specifically
“good” species (eine spezifisch “gute”
Art). His description fits M. arenaria
except for the cartilage tooth which he
describes as resembling that of M. trun-
cata, a fact already pointed out by Jensen.
It would seem that his only point is that:
“M. ovata Jensen homonym mit Donovan
(1802, pl. 122) (=Unio tumidus Retz.) ist
and daher durch einen neuen Namen
ersetzt werden muss”. But even here
it is difficult to follow Schlesch; first
of all because Jensen himself never con-
sidered M. truncata forma ovata a
Species or even a subspecies and never
called it “М. ovata”, as quoted by
Schlesch. For that reason the change
of name is irrelevant. What Schlesch
really did was toarbitrarily raiseaform
to species level, without proofs, and
then change its name.
The present author worked with Jensen
for a number of years. We discussed
the taxonomy of Mya truncata forma
ovata on several occasions. It was
Jensen’s opinion that forma ovata could
not be more than an infrasubspecies. As
work proceeded (Harder, Jensen &
Laursen, 1949) and evidence was col-
lected of the intergradation between M.
truncata f. uddevallensis and M. truncata
f. typica on the one hand, and of M. trun-
cata f. ovata and M. truncata f. typica on
the other, the validity of Jensen’s opinion
was further corroborated.
Schlesch (1931: 137) quotes Brégger
(1900/01: 608) as stating (in Norwegian)
(with regard to the form ovata): “It is
a specific form closest to M. truncata.”
Schlesch, however, picks out only part
of Brégger’s statement (р 607-608),
which, translated from the Norwegian,
runs as follows: “Mya arenaria was
until now generally considered anArctic
ARCTIC MYA 411
species; however in a paper recently
published, Ad. S. Jensen demonstrated
that the Mya specimens from Arctic
coasts, recorded earlier as Mya aren-
aria, actually do not belong to that
species, but are a specific form related
to Mya truncata, if anything, and by
Jensen indicated as Mya truncata forma
ovata, whereas Mya arenaria turns out
to be a typical boreal form . ..”. Brog-
ger then gives information about the
distribution of M.arenaria. As can
be seen, Brógger merely quotes Jensen—
and agrees with him. Since Schlesch
wrote his paper, some malacologists
have accepted the name M. pseudoaren-
aria without hesitation whereas others
have discussed the problem before they
decided which name to use.
Hessland (1943) does not deal with
the problem, but has some interesting
observations concerning Mya truncata,
which are worth mentioning here be-
cause they settle the arguments about
range and distribution of thick and thin-
shelled Mya truncata forma typica and
Mya truncata forma uddevallensis.
During field work for his doctor’s thesis
on the Pleistocene in southwestern
Sweden, he came upon a very well pre-
served Mya-biotope in clay in which
both the typical form and the udde-
vallensis form were present in great
numbers. The shells-showed a complete
series of intermediate forms between
typical M. truncata and forma uddeval-
lensis. Furthermore, Hessland observed
that the supposedly southern, protracted,
thin-shelled form occurred abundantly
with the thick-shelled, truncated, typical
form and with forma uddevallensis, both
believed to indicate a relatively cold
water temperature.
This author (Laursen, 1944, 1945,
1950, 1954), in examining large col-
lections of fossil shells from West
Greenland and some from Canada, found
a complete transition between M. trun-
cata and its 2 extreme forms. The new
material dealt with in this paper also
indicates the same trend, even if the
number of shells concerned is limited.
A reexamination of shell material avail-
able in Scandinavian museums from
localities in the Eastern hemisphere did
not give evidence for the correctness of
establishing forma ovata as a distinct
Species. In my opinion the differences
in the shells of the 2 forms are not
enough to establish a new species.
Foster (1946) mentions the ovata form
but refers to it as Mya pseudoarenaria
Schlesch. Apparently, he did not in-
vestigate the problem. He thinks of
“Mya pseudoarenaria” as the Arctic
counterpart of М. arenaria, which is
not correct.
Soot-Ryen (1951) thinks Schlesch is
correct in his assumption, although the
Species of Mya are polymorphic and a
thorough revision is needed of the vari-
ous forms, both living and fossil, in the
Northern Pacific.
Feyling-Hanssen (1955a), in his ex-
cellent paper on the marine Late-
Pleistocene of West Spitsbergen, in-
vestigated a great number of Mya trun-
cata shells including both forma ovata
Jensen and forma uddevallensis Forbes.
He maintains (p 150) the classification
set forth by Jensen because of the
transitions occurring between the typical
and extreme forms. The transitions
are shown in 3 diagrams.
Ockelmann (1958), in an extensive and
excellent paper, has examined the large
collection of recent Mya shells from
East Greenland kept in the Zoological
Museum of Copenhagen. He (p 148)
arrives at the same results as do
Feyling-Hanssen and the author: “Be-
tween f. ovata and the typical M. trun-
cata all grades of transitional stages
occur”. Ockelmann also has his doubts
about forma ovata being a subspecies.
Until further proof is given I suggest
that the name Mya pseudoarenaria
Schlesch not be used.
ACKNOWLEDGMENTS
The author is indebted to Dr. Frances
J. E. Wagner of the Geological Survey
of Canada, to Dr. D. J. McLaren, Head
412 D. LAURSEN
of the Palaeontology Section and to Dr.
J. F. Calez, Chief of the Division of
Fuel and Stratigraphy for lending him
the new material used for this paper.
I especially want to thank Dr. Wagner,
Dr. D. F. Hewitt, Senior Geologist of
the Department of Mines, Toronto, On-
tario, and Dr. L. G. Berry of Queen’s
University, Kingston, Ontario, for their
valuable help in tracing the old col-
lection from the Hudson Bay Area.
I am very grateful to Dr. Horace
G. Richards, Academy of Natural Science
of Philadelphia, and Dr. Harald A.
Rehder, U. S. National Museum,
Washington, D. C., because they took
time to reexamine and review earlier
identifications.
Dr. Rolf Feyling-Hanssen, Palæon-
tologisk Museum, Oslo, Norway,
confirmed, on my request, that the data
from Norway and Spitsbergen were un-
changed; he and Mr. Jgrgen Knudsen,
M.Sc., Zoologisk Museum, Copenhagen,
Denmark, provided me with shell
material for comparisons. Their help
is highly appreciated.
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mollusca and brachiopoda from Spitz-
bergen. Tromsg Mus. Arsh., 47:
1-10.
, 1932, Pelecypoda, with adis-
cussion of possible immigrations of
Arctic pelecypods in Tertiary times.
Norw. North Polar Exp. “Maud”, 1918-
1925. Sci. Results, 5(12): 1-35.
, 1939, Some pelecypods from
Franz Josef Land, Victoriagya, and
Hopen collected on the Norwegian
Scientific Expedition 1930. Medd.
Norges Svalb. Ish.-Unders., (43):
1-22 +1 pl.
, 1951, New records onthe dis-
tribution of marine Mollusca in
northern Norway. Astarte, 1: 11 p.
SPARCK, R, 1933, Contribution to ani-
mal ecology of the Franz Joseph
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1-38.
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‘ lections. Contr. Canad. Biol. 1906-
1910, p 221-242.
SVERDRUP, H. V., JOHNSON, M. W., &
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THORSON, G., 1934, Investigations on
shallow water animal communities in
417
the Franz Joseph Fjord (East Green-
land) and adjacent waters. Medd. om
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, 1936, The larval development,
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rine bottom invertebrates. Medd. om
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arenaria japonica. Venus, 8: 13-21.
EL GENERO MYA EN LA REGION ARTICA
El presente trabajo tiene por objeto clarificar conceptos erröneos acerca de las
especies articas de Mya. Jensen sefialö (1900, en dinamarqués) que todas las refer-
encias hasta entonces existentes de M. arenaria Linnaeus para el Artico eran equivo-
cadas, y correspondian en realidad a una forma de M. truncata Linnaeus, que el llamó
ovata. La distinción más notable entre las conchas, casi similares, de las dos especies,
se encuentra en los cartilagos de la placa en la valva izquierda y la fosa, correspond-
iente al cartilago, de la valva derecha. Sin embargo, como la publicaciön de Jensen
418
D. LAURSEN
es poco conocida en el mundo de habla inglesa, M. arenaria, una especie boreal, se
sigue señalando para al Artico. Además, Schlesch (1931) elevó arbitrariamente
ovata, la cual Jensen consideraba cuando más una infrasubspecie, a la categoria de
especie, y la redenominó M. pseudoarenaria, nombre que no debe ser usado.
Se da aquí la distribución, Reciente y fósil, de tres formas de M. truncata: forma
typica Linnaeus, M. truncata forma uddevallensis Forbes, y M. truncata forma ovata
Jensen. La distribución de M. arenaria también se da hasta donde es conocida. Las
listas no son completas. A los investigadores que trabajan con M. truncata se les
solicita dar más detalles en el futuro acerca de las formas.
Se discuten algunas nuevas localidades dadas para M. arenaria, dentro de la región
Artica, todas las cuales corresponden a M. truncata f. ovata.
age
MALACOLOGIA, 1966, 3(3): 419-431
STATOCYST FUNCTION IN POMACEA PALUDOSAl
(MESOGASTROPODA: AMPULLARIIDAE)
Andrew McClary
Department of Natural Science
Michigan State University
East Lansing, Michigan, U.S.A.
ABSTRACT
Two groups of snails were studied. Group I consisted of 15 snails from which
the left statocyst had been removed, 15 sham-operated snails in which the left
statocyst had been exposed by operation but left intact, and 15 unoperated con-
trols. Group II consisted of 8 snails from which both statocysts had been re-
moved, 8 doubly-sham-operated snails and 8 controls. Prior to operation,
snails were anesthetized by submersion for approximately 1 hour in . 25g/liter
of MS 222. Wound closure was rapid, and snails became active within an hour
after operation. Later autopsy gave no indication of statocyst regeneration.
Studies were made of the following behavior patterns: rate and direction of
movement, activity level, position when at rest, ability to right after inversion,
ciliary feeding and surface inspiration.
During these studies, some GroupII operated and sham-operated snails showed
an abnormal sagging of the shell. During the activity level studies on Group I,
operated and sham-operated snails were less active and less ableto rest on ver-
tical surfaces than controls. The above changes were considered due to opera-
tive incision.
During activity level studies on Group II, operated snails were less able to rest
on vertical surfaces than sham-operated or control snails, and this was interpre-
ted as due to statocyst removal.
Other than the above, no significant behavioral differences occurred between
operated and sham-operated snails and their controls.
Snails lacking both statocysts showed no loss in ability to move to the water’s
surface to inspire.
Among the potential factors governing direction to the surface in the absence of
statocysts, overhead light and oxygen gradients were presumably eliminated by
lateral light and circulation of water. Limited experiments suggested that ten-
sion induced by the pendant shell did not provide a cue, as twisting the shells of
moving snails failed to divert their upward movement. Potential cues which re-
mained were pressure gradients and lung buoyancy.
INTRODUCTION died (Carthy, 1958; Fraenkel & Gunn,
1961), experimental work on the func-
Although the role of statocysts in tion of gastropod statocysts is limited.
other invertebrates has been amply stu- A few workers have shown that stato-
i cae Me Е
This investigation was supported by National Science Foundation grant NSF-G-19373. I wish to
thank Richard Herrmann, now at the School of Medicine, University of Wisconsin-Madison, for
his invaluable help as a project assistant during the course of this work.
(419)
420 A. McCLARY |
cysts function in the static orientation
and horizontal movement of snails. Thus,
removal of a statocyst from the hetero-
pod Pterotrachea resultedinatemporary
rolling on the longitudinal axis and a
loss of tonus (Tschachotin, 1908; Fried-
rich, 1932). Interruption of a single
statocyst nerve of the tectibranch Aply-
sia caused a circus movement; interrup-
tion of both, a general loss of equili-
bration (Pelseneer, 1935). Removal of
one pedal ganglion with its associated
statocyst from the pteropod Cymbulia
caused irregular movement towards the
operated side and a similar effect was
obtained with Helix pomatia (Pelseneer,
1935).
Although light (Kanda, 1916a, b; Fraen-
kel, 1927; Crabb, 1929) and muscle ten-
sion (Davenport & Perkins 1897; Frand-
sen, 1901; Kanda, 1916a; Cole, 1925;
Crozier & Navez 1930; Hoaglund & Cro-
zier 1931; Bower, 1962) have commonly
been considered to direct the movements
of gastropods on vertical surfaces or
slopes, statocysts may also function in
this way. Thus, in a study of down-
ward motion on an inclined plane, Lever
& Geuze (1965) have recently demon-
strated disorientation of the aquatic pul-
monate snail Lymnaea stagnalis after bi-
lateral statocyst extirpation, and, after
unilateral extirpation, some deviation
towards the side of the remaining stato-
cyst.
The present paper reports the effect
of statocyst removal on certain behav-
ioral patterns of the prosobranch Po-
macea paludosa. This species was chosen
FIG. 1. Method of extension of animal for stato-
cyst removal. Arrow indicates approximate
location and size of incision.
for study as it is easily maintained in the
laboratory, possesses statocysts acces-
sible to operative removal (McClary,
1963) and has been the subject of stud-
ies on behavioral patterns suspect of
statocyst control (Johnson, 1952;
McClary, 1964).
GENERAL METHODS
A laboratory population of marked
snails was maintained in glass aquaria
with charcoal filtered, continuously cir-
culating tap water at about 260 С+2,
as previously described (McClary, 1964).
The animals were 170 days old and
weighed an average of 5.6 g at initia-
tion of studies. The behavior of 2
TABLE 1. Post-operation survival rates of Pomacea paludosa 4 days after removal or exposure
of statocysts
Category
I
unilaterally
operated
II
bilaterally
operated
Removed
Sham operated
Removed
Sham operated
16 15
15 15
11 8
10 8
% recovery
94
100
73
80
STATOCYST FUNCTION IN POMACEA
groups was studied. Group I consisted
of 15 snails from which the left stato-
cyst had been removed, 15 sham-
operated snails, and 15 controls. Group
II consisted of 8 (later 7, after death
of one) snails lacking both statocysts,
8 doubly sham-operated snails, and 8
controls.
Operations were performed as follows:
subjects were anesthetized by immersion
in .25 g/liter of MS 2222 until animals
could be extended manually from their
Shells, though still exhibiting some mus-
cle tension. Required immersion time
averaged one hour.
One worker then held the anesthetized
snail by its shell and pulled the oper-
culum down toward the shell apex. This
forced the animal to partially extend
from the shell. A second worker made
a shallow lateral incision on the left
side of the body wall (Fig. 1). A suc-
cessful incision exposed the statocyst,
which lies approximately 2 mm below the
surface and is easily identified by its
refractile statoliths. The statocyst was
then removed with fine forceps and
checked under a dissecting microscope.
Whenever a statocyst was broken, or
carried adherent tissue, the snail was
discarded. If removal was successful,
the snail was placed in a 20 gallon
recovery tank, and normally became ac-
tive within an hour. Wound repair was
typically rapid and without complica-
tions, the incision being completely
healed after a week. When both stato-
cysts were scheduled for removal, an
operation was performed successively on
each side of the snail. Insham-operated
snails statocysts were exposed as above
but not removed. This was done so
that effects of simple incision could be
RA methanesulphonate, available from
Sandoz Pharmaceuticals, Hanover,
U. S. A. I wish to thank Profs. H. van der
Schalie for suggesting MS 222 as a suitable
anesthetic, and J. Lever for advice regarding
its use.
МЫ;
421
FIG. 2. Surface inspiration Бу Pomacea palu-
dosa, as viewed through aquarium wall. Typi-
cal posture is shown at A, detail of head and
siphon at B.
distinguished from effects of statocyst
removal. Table 1 gives data on opera-
tions.
After operations, snails were allowed
to recover for at least 4 days. The
behavior patterns which follow were then
studied. (The time lapse between opera-
tion and study commencement is in pa-
renthesis): surface inspiration (GpI, 12-
14 days; Gp I, 14-20 days), ciliary
feeding (Gp I, 19 days; Gp II, 9 days),
activity level (Gp I, 4-6 days; Gp II,
8-9 days), rate and direction of move-
ment (Gp I, 10 days; Gp II, 10 days),
ability to upright themselves after in-
version (Gp II, 14 days). At completion
of the studies, all snails were killed
and examined for statocysts. No evi-
dence of regeneration was found inthose
Snails from which statocysts had been
removed.
422 A. McCLARY
RESULTS OF STUDIES
Surface Inspiration
Impending surface inspiration can
usually be anticipated, for prior to it,
and while still moving upward to the wa-
ter’s surface, P.paludosa will commonly
form its left mantle lobe into a long,
tubular siphon. Upon reaching the sur-
face, the snail normally first contacts
the air-water interface with its left ten-
tacle. - The siphon is then brought into
contact with the interface, and air is
pumped by a series of body contrac-
tions to a lung situated in the mantle
cavity (Fig. 2). After inspiring, P.
paludosa typically turns down toits right
and either drops or crawls to the bottom
of the container (McClary, 1964).
Surface inspiration was studied in 2
oilcloth wrapped glass cylinders meas-
uring 46 x 21 cm which contained
aerated circulating water at 26°C, as
described for control cylinders in my
previous (1964) work, except that lateral
rather than overhead illumination was
used, light entering through slits in the
oilcloth. Snails of Groups I and II were
studied in separate cylinders. For any
one observation, 4-5 snails of each cate-
gory were placed in a cylinder at 09:30
and watched for 2 hours. All snails of
Group I were observed twice; those of
Group Il, 6 times. During observations,
the following data were recorded:
TABLE 2.
Structure first
contacting surface*
Left aie
Si
Total
No. of
inspira-
tions
Category
(15 each)
Left
statocyst
removed
Sham
operated
Control
1. All surface inspirations. On oc-
casion a snail remained at the wa-
ter’s surface between inspirations.
When this happened, the second in-
spiration was not added to the data,
for frequency of surface inspiration
was intended to serve as ameasure
of the snail’s ability to move up-
wards to the surface.
2. The number and location, at 10
minute intervals of all inactive
snails.
3. The behavior of snails of Group I
during surface inspiration.
4. Tracks made prior to inspiration by
several snails of Group II. Records
were begun when a snail was in the
lower half of a cylinder and were
made by observing the snail’s move-
ment from above the cylinder and
pressing a mark into the oilcloth
so as to record the snail’s track.
Table 2 summarizes the behavior of
Group I during surface inspiration. In
all 3 categories of this group, behavior
of snails was similar to that observed
in the previous study. No data were
taken on behavior of Group П during
surface inspiration. However, informal
observations suggested that the behavior
of this group was normal except that 2
operated and 2 sham-operated snails had
apparently lost some control over their
Shells; for the latter tended to sag away
Behavior of 15 Group I snails during surface inspiration
Direction
Average Behavior
A turned
contractions after
after As
per : ce ИЕ turning
: AR inspiration*
inspiration
*indicates that data are not available for all inspirations
STATOCYST FUNCTION IN POMACEA
TABLE 3.
423
Frequency of surface inspirations in Pomacea paludosa after statocyst removal. *
Snails of Group I were observed a total of 4 hours, those of Group П, 12 hours.
t values insignificant at . 05 level of rejection
All
Average
Number of Standard Student’s
x Total number of IR
Group Category snails и. SEE deviation T-test
inspirations | inspirations
observed Г (3) (t)
per snail
Removed
y : Sham
unilaterally Я
operated P
Control
Removed
I
bilaterally F m d
operated P
Control
*measures frequency of motion towards surface
from the body, particularly when a snail
was moving on a cylinder wall.
As indicated in Table 3, the inspira-
tion frequency of operated and sham-
operated snails in each group did not
differ significantly from that of con-
trols. Snails of both groups remained
inactive for extended periods, and the
over-all frequency of surface inspiration
was markedly lower than that found in
my earlier study (McClary, 1964). No
attempt was made to analyze the cause
for this, although it is suspected that
seasonal differences between the studies
may have been a Contributing factor.
The tracks (Fig. 3) made by snails of
0.0
Group II prior to inspiration suggested
a directed rather than a random move-
ment to the surface. To test this,
drawings of each track were placed on
а 1 cm2 grid, and the number of ver-
tical vs. horizontal line crossings com-
pared. Chi square analysis of the data
is shown in Table 4. As indicated by
the table, operated snails showed a di-
rected movement tothe surface, although
both statocysts had been removed.
As cylinder water was in circulation
during all observations, the possibility
that an oxygen gradient acted as the
necessary cue to this movement was
eliminated. Since lateral light was used,
TABLE 4. Analysis of surface directed tracks, made by Group II snails, superimposed on a
2 .
cm# grid
Number
of
tracks
Category lines
Both statocysts
removed
Sham operated
Control
Horizontal
crossed
Vertical Total
lines lines 2*
X
crossed crossed
8.82
*All X2 values significant at . 05 level of rejection, i.e. , movement is directed
424 A. McCLARY
N
OPERATED
17
SHAM OPERATED
\
CONTROL
5cm
FIG. 3. Typical upward tracks made by snails
of Group I prior to surface inspiration.
which entered each cylinder approxi-
mately halfway from the topthrough slits
in the oilcloth, it seemed unlikely that
light could have acted as a cue.
Various workers (Frandsen, 1901;
Kanda, 1916a; Cole, 1925; Crozier &
Navez, 1930; Hoaglund & Crozier, 1931)
have suggested that shell muscle tension
acts to direct vertical movement in
gastropods. Thus, Crozier & Navez
(1930) found that Liguus, a tree snail
which normally moves vertically, could
be diverted from upward movement by
twisting the shell out of alighment with
the body. When this was done, Liguus
would change its path of travel from the
vertical until shell and body were again
aligned and shell muscle tension was
equal on both sides. If shell muscle
tension guided Pomacea upward, it was
thought that a similar diversion would
result from twisting the shell. Accor-
dingly, threads were affixed to the shell
apices of several Group II snails. When
a snail moved upward, and signaled in-
tent to inspire by siphon extension, its
shell was pulled out of alignment with
the body. As shown in Fig. 4, twisting
the shell of these snails failed to di-
vert them from their upward travel.
Thus, limited experiments failed to sup-
port the possibility that shell muscle
tension provided the stimuli for the ver-
tical movement of P. paludosa.
Ciliary Feeding
In the presence of particulate food on
the water’s surface, P. paludosa will
shape the anterior region of its foot into
a funnel and, by means of ciliary ac-
tion, collect the food contained in the
surface film. The aggregated food,
mixed with mucus, is then concentrated
under the rear portion of the foot and
ingested at intervals (Johnson, 1952;
McClary, 1964). Typical feeding posture
is shown in Fig. 5.
The effect of statocyst removalon cil-
iary feeding posture was studied by pla-
cing snails in 5-gallon aquaria that were
illuminated laterally and half filled with
filtered tap water at 26°C, and by adding
a small amount of particulate food tothe
surface.
STATOCYST FUNCTION IN POMACEA
3cm i
FA for
* A
| Ni :
Ся / ‘à !
Mi has! -
i a :
\ : 47
i
Ir
OPERATED SHAM CONTROL
OPERATED
FIG. 4. Typical results of twisting shells
during movementto surface. Tracks selected
from approximately 5 records for each cate-
gory. All snails from Group II. Arrows in-
dicate directionin which shell apex was pulled;
dotted line, period during which pull was ex-
erted. Shells were twisted approximately 300
from body axis.
In 3 operated and 2 sham-operated
snails of Group II, a tendency existed for
the shell to sag away from the aquarium
wall while the snail was feeding. Two of
the 3 operated snails had showna similar
behavior while rising to inspire. Apart
from these, all snails showed a normal
posture during ciliary feeding.
Activity Level
The general procedure for studying
activity level was similar to that of
previous work (McClary, 1964). Two
plastic dishes approximately 10 cmdeep
were used. Each contained 3,200 cc of
filtered water at 26°C and was illumi-
nated by overhead fluorescent light. In
the study of GroupI, 15 snails were placed
in each dish; for Group II this number
was reduced to 12. In each case, dishes
contained approximately equal numbers
of operated, sham-operated and control
snails. All snails were watched for 2
two-hour periods, during which a record
was made at 5 minute intervals of all
inactive snails and their position in
425
dishes.
In addition to the results of this study,
data on number and location of inactive
snails were available from that on sur-
face inspiration.
Tables 5 and 6 show results of these
studies. During the activity level study
on Group I, operated and sham-operated
Snails showed a significant decrease in
activity, and in ability to rest on verti-
cal surfaces. During both activity level
and surface inspiration studies on Group
II, operated snails showed a significant
loss of ability to rest on vertical sur-
faces.
Rate and Direction of Movement
Snails were tested in 3,000 cc plastic
dishes containing filtered tap water at
26°C. Illumination was by overhead
fluorescent light. Each snail (7-10from
each category) was tested singly for 5
FIG. 5. Typical posture assumed by Pomacea
paludosa during ciliary feeding. Animal as
viewed through aquarium wall. Arrow indi-
cates food-mucus aggregate under posterior of
foot.
426 A. McCLARY
TABLE 5. Activity level of Pomacea paludosa after statocyst removal, recorded at 5-10 min-
ute intervals 4
Number
snails
used
Group Study Category
Removed
Activity Sham
level operated
I Control
unilaterally
Removed
operated
Surface Sham
inspiration | operated
Control
Removed
Sham
operated
Activity
level
A Control
bilaterally
Removed
operated
Surface Sham
inspiration | operated
Control
Number of |Average No. of | Standard | Student’s
observations
per snail
observations | deviation
as inactive (t)
0. 38
2.08
1.61
*indicates significant difference from control at . 05 level of rejection
minutes and its track onthe bottom ofthe
dish, which was transparent and marked
with a grid, was recorded as previously
described (McClary, 1964). Each snail
was observed once. Typical tracks are
shown in Fig. 6A € В. Table 7 indicates
that there was no significant difference in
rate of movement amongthe categories of
each group. Although some increase in
turning Was present in tracks of Group I
operated snails (Fig. 6A, Table 7), there
was no conclusive evidence of any true
circus movement. Three operated and
2 sham-operated snails of Group II tended
to move with their shells sagging to the
right. These were the snails which
showed a similar behavior in the ciliary
feeding study.
Ability to turn over when inverted
Limited observations were made to
determine whether snails of Group II
could right themselves. Snails were
placed individually, operculum upwards,
in water-filled finger bowls. An initial
test employed lateral fluorescent lights.
Snails were observed for 1 hour. At
the end of this period, 4 of 7 operated,
2 of 8 sham-operated, and 1 of 8 con-
trol snails had succeeded in righting
themselves as a result of the animal’s
efforts while extending from the shell.
In addition, 3 sham-operated and 3 con-
trol snails remained retracted, but rolled
over.
In a second test, similar to the first,
except that it was conducted in complete
darkness, the following number of ani-
mals were found to have righted them-
selves after 1 hour: operated, 5 of 7;
sham-operated, 8 of 8; control, 6 of 6.
Thus, there was no indication that loss
of statocysts caused any significant de-
crease in ability to right, either in light
STATOCYST FUNCTION IN POMACEA 427
TABLE 6.
Number
snails
Group Study Category
used
Removed
Sham
operated
Activity
level
1 Control
unilaterally
R
operated =e
Sham
operated
Surface
inspiration
Control
Removed
Sham
operated
Activity
level
2 Control
bilaterally
R
‚ operated о.
Surface Sham
inspiration] operated
Control
observations
when snails
Position of inactive snails, indicating reduced ability to rest on vertical surfaces
after bilateral statocyst removal
Position when observed
On On
vertical horizontal
surface surface
Total
inactive
*indicates significant difference from control at . 05 level of rejection
or darkness.
DISCUSSION
Previous studies which have involved
experimental extirpation or neutraliza-
tion of statocysts (Tschachotin, 1908;
Friedrich, 1932; Pelseneer, 1935; Lever
& Geuze, 1965) demonstrated a disrup-
tion of normal behavior.
In contrast, the present study pro-
duced no evidence that statocysts are
necessary for the maintenance ofnormal
behavioral patterns in P. paludosa, al-
though the data can only be regarded as
tentative duetothe small population used.
The only behavioral change in the pre-
sent work which appeared to relate to
statocyst loss was the decreased ability
of Group II bilaterally operated snails to
rest on vertical surfaces. The decrease
in activity and in ability to rest on ver-
tical surfaces shown by GroupI operated
snails of the activity level study was
probably due to operative incision rather
than to statocyst loss, since a similar
reduced capability also occurred with
sham-operated snails. Asthis study was
the first to be conducted, and began only
4 days after operations were concluded,
it seems likely that the reduction in
activity and in ability to rest on verti-
cal surfaces was due to incomplete wound
healing. The sagging of shells found
428 A. McCLARY
SNE
OPERATED
rt roe
SHAM OPERATED
(695
CONTROL
A 5cm
5
$
$
ES =
OPERATED
LAG
SHAM OPERATED
Сре
CONTROL
5 ст
В
in both operated and sham-operated
snails of several studies was presum-
ably a result of a similar but longer
lived damage from operation.
It is suggested that the discrepancy in
results between the present and previous
studies may be due to several factors.
In some earlier studies, behavioral ab-
normalities may have resulted from ge-
neralised operative damage. This would
seem particularly likely in the case of
those experiments on Cymbulia and He-
lix (Pelseneer, 1935) in which the entire
pedal ganglion was removed. In other
experiments such as those onheteropods
(Friedrich, 1932), observed abnormali-
ties apparently were transient in nature.
This suggests that similar transient be-
havior patterns may appear when stato-
cysts are removed from Pomacea, but
were missed in the present study due
to the time lapse between operation and
observation. The differences between the
results of Lever and Gauze (1965) with
Lymnaea and those ofthe writer with Po-
macea may be a reflection of the numbers
of Pomacea studied, differences in time
lapse between operation and experiment,
or possibly real differences relative to
the species used.
In Pomacea, normal behavior with res-
pect to substrate orientation, horizontal
movement, feeding posture and surface
inspiration could presumably have been
maintained despite the absence of stato-
cysts through contact and visual stimuli.
With respect to vertical movement, a
number of cues to direction other than
those provided by statocysts could have
been used. Some of the more likely are
as follows:
1.) Gravity acting on shell muscle.
As suggested by Crozier and others
(Crozier & Navez, 1930), vertical move-
ment of gastropods may result from an
adjustment of position until shell muscle
tension on both sides of the body is
FIG. 6. Typical horizontal tracks made by
snails during study of rate and direction of
movement. А =GroupI, В = Group П. S in-
dicates start of 5-minute run.
STATOCYST FUNCTION IN POMACEA 429
TABLE 7. Rate and direction of movement on horizontal surface
Group Category
Left statocyst
removed
Sham
operated
Control
Both statocysts
removed
Sham
operated
II
Control
*All t values insignificant at . 05 level of rejection
equal, as would occur when shell and
body are aligned on a vertical axis.
However, various workers have criti-
cized the studies on whichthisidea rests
(Hunter, 1931; Fraenkel & Gunn, 1961),
and the “string and apex” tests of the
present study also argue against it as
a means of orientation for Pomacea.
2.) Weight of the shell. As suggested
by Fraenkel & Gunn, the upward move-
ment of gastropods may be passive in
nature; the weight of shell forcing the
body to orient vertically. However, it
is again difficult to reconcile the string
and apex experiments of the present
study with this idea, and at least one
gastropod, Physa integra, is able to carry
out directed vertical movement when
suspended in a viscous medium which
presumably eliminates any weight effect
(McClary, 1961).
3.) Light. Although, in the present
work, Group II snails moved vertically
in the absence of overhead light, it is
possible that the lateral light used pro-
duced refraction patterns either on the
cylinder walls or air-water interface,
and that these served as cues to up-
ward movement.
Average
distance
traveled
per snail
(in cm)
Total number of
360° turns
Student’s
T-test
(t)*
Standard
deviation
(s)
To left To right
4.) Pressure of the ambient medium.
Although theoretically valid, the minute
pressure differences to be found along
an animal of the size of Pomacea coupled
with the apparent lack of any pressure
receptors, makes this mode of detection
rather unlikely.
5.) Gas in the lung. The location of
the lung within the mantle cavity of Po-
macea is such that its buoyancy could
tend to cause snails to travel upward
on a vertical surface. Although lung
gas is reduced prior to surface inspira-
tion (McClary, 1964), it is conceivable
that enough buoyancy still remains to
produce such an effect.
REFERENCES
BOWER, D. R, 1962, A new method of
determining the accuracy of geotactic
orientation of the snail Helix aspersa
Müller. Veliger, 4(4): 181-184.
CARTHY, J. D., 1958, An introduction
to the behavior of invertebrates. The
Macmillan Co. New "York, N.'Y.
COLE, W. H., 1925, Geotropism and
muscle tension in Helix. J. gen.
Physiol., 8: 253-263.
430 A. McCLARY
CRABB, E. D., 1929, Egg laying and
birth of young in three species of
Viviparidae. Nautilus, 42(4): 125-129.
CROZIER, W. J. & NAVEZ, A. E., 1930,
The geotropic orientation of gastro-
pods. J. gen. Psychol., 3: 3-37.
DAVENPORT, C. B. & PERKINS, H.,
1897, A contribution to the study of
geotaxis in higher animals. J. Physiol.
22: 99-110.
FRAENKEL, G., 1927, Beiträge zur
geotaxis und phototaxis von Littorina.
Z. vergl. Physiol., 5: 585-597.
& GUNN, D. L., 1961, The
orientation of animals. Dover Publ.
New York, N. Y.
FRANDSEN, P., 1901, Studies on the
reactions of Limax maximus to di-
rective stiumli. Proc. Amer. Acad.
Arts Sci., 37: 185-227.
FRIEDRICH, H., 1932, Studien tiber die
Gleichgewichtserhaltung und Beweg-
ungsphysiologie Pterotrachea. Z.
vergl. Physiol., 16: 345-361.
HOAGLUND, H. & CROZIER, W. J.,
1931, Geotropic excitation in Helix.
J. gen. Physiol., 15(1): 15-28.
HUNTER, W. S., 1931, The mecha-
nisms involved in the behavior of
white rats on the inclined plane. J.
gen. Psychol. 5: 295-310.
JOHNSON, В. M., 1952, Ciliary feeding
fresh-water snails. Jbid.
in Pomacea paludosa.
1-5.
KANDA, S., 1916a, Studies on the geo-
tropism at the marine snail Littorina
littorea. Biol. Bull., 30: 57-85.
, 1916b, The geotropism of
30: 85-
Nautilus, 66:
97.
LEVER, J. € GEUZE, J. J., 1965,
Some effects of statocyst extripations
in Lymnaea stagnalis. Malacologia,
2(3): 275-280.
McCLARY, A., 1961, Apparent geotac-
tic behavior in Physa. Nautilus, 75
(2): 75-79.
, 1963, Statolith formation in
Pomacea paludosa (Say). Amer.
malacol. Union. Ann. Repts., 30: 20-
21.
, 1964, Surface inspiration and
ciliary feeding in Pomacea paludosa
(Prosobranchia: Mesogastropoda:
Ampullariidae). Malacologia, 2(1):
87-104.
PELSENEER, P., 1935, Essai d’Eth-
ologie zoologique d’apres. l’étude des
mollusques. Publ. Fond. Agnathon
Potter, No. 1. Palais des Acadé-
mies. Bruxelles.
TSCHACHOTIN, S., 1908,
cyste der Heteropoden.
Zool., 90: 343-422.
Die Stato-
Z. wiss.
RESUMEN
FUNCION DEL ESTATOCISTO EN POMACEA PALUDOSA
(AMPULLARIDAE)
Se estudiaron dos grupos de caracoles. El grupo I consistió de 15 ejemplares a
los cuales se les extirpó el estatocisto izquierdo, otros 15 en los que se efectuó
una pseudo-operaciön para exponer el estatocisto izquierdo sin extirparlo, y final-
mente 15 quedaron sin ser operados para control. En el grupo Па 8 caracoles se le
extirparon ambos estatocistos, 8 fueron pseudo-operados, y 8 de control.
Los caracoles fueron anestesiados, por sumersión aproximadamente de una hora,
en 25g/litro de MS 222. El cierre de la incisión fué rápido, y los caracoles reasum-
ieron actividad dentro de una hora después de la operación. Autopsia posterior no
indicó regeneración de estatocistos.
Se estudiaron los siguientes comportamientos: velocidad y direcion del movimiento,
nivel de actividad, posición de descanso, habilidad correctiva despues de la inversión,
alimentación ciliar e inspiración superficial.
Algunos ejemplares operados y pseudoperados del grupo II mostraron abollamiento
normal de la concha. El nivel de actividad de los caracoles del grupo I fué menor,
e incapaces de descansar, comos los controles, sobre superficies verticales. Estos
STATOCYST FUNCTION IN POMACEA
cambios deben considerarse como causados por la incisión operativa. La extir-
pación de estatocistos en el grupo II causó el mismo efecto que en el I.
Otras diferencias observadas en el comportamiento entre los operados y los
controles no fueron significativas.
Caracoles desprovistos de ambos estatocistos no mostraron disminucion en la
habilidad para trasladarse e inspirar en la superficie del agua. Entre los factores
potenciales que gobierna la dirección a la superficie y la ausencia de estatocistos,
luz desde arriba y gradientes de oxígeno fueron presumiblemente eliminados por luz
lateral y circulación del agua.
431
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MALACOLOGIA, 1966, 3(3): 433-439
EVOLUTIONARY AND SYSTEMATIC IMPLICATIONS OF
A TRANSITIONAL ORDOVICIAN LUCINOID BIVALVE
A. Lee McAlester
Department of Geology, Yale University
New Haven, Connecticut, U. 5. A.
ABSTRACT
Stratigraphic and morphologic evidence indicate that the rare Ordovician bi-
valve Babinka is an evolutionary transition between the bivalve superfamily
Lucinacea and some monoplacophora-like ancestral mollusc. Paleontologic evi-
dence and comparative functional studies of recent forms suggest that the Lucin-
acea, Leptonacea and Babinka represent an independent evolutionary lineage
which has maintained unique adaptive features since early Paleozoic time. This
lineage should probably be treated as a separate bivalve taxon of the highest
rank. Lucinoids do not appear to have given rise to other major groups of bi-
valves and are probably unrelated to most other “heterodont” forms with which
they are commonly associated. The independent origin of lucinoid bivalves
suggests that the Bivalvia had a polyphyletic origin from non-bivalved ancestral
molluscs.
INTRODUCTION
Since the recognition of the signifi-
cance of the multiple muscle scars in
early fossil representatives of the class
Monoplacophora, andthe subsequent dra-
matic discovery of the living monoplaco-
phoran Neopilina, there has been a search
by paleontologists for other early fossil
molluscs with multiple muscle scars
which might indicate a relationship to
the Monoplacophora. Of particular
Significance would be the discovery of
fossils representing the transition be-
tween some monoplacophora-like an-
cestor and any of the other molluscan
classes, but as yet the search for such
transitional fossils has yielded few re-
sults. One fossil which has attracted
wide attention as a possible transitional
form is the rare bivalve genus Babinka,
which was first described by Barrande
in 1881. The genus is known primarily
from about a 100 specimens found in
lowest Middle Ordovician (Llanvirn)
rocks of the Bohemian Basin near
Prague, Czechoslovakia. Barrande’s
original figures showed that these speci-
mens have a peculiar series of elongate
muscle-scar impressions on the dorsal
region of the valve interiors, and this
pattern led Vokes (1954) to suggest that
Babinka might be a transition between
the Bivalvia and a monoplacophora-like
ancestral mollusc. Vokes’ suggestion
was quickly taken up by other students
of bivalve phylogeny, and the genus has
been widely regarded an an ancestral
bivalve (Cox, 1959, 1960; Ruzicka &
Prantl, 1960; Horny, 1960; Vogel,
1962; Merklin, 1962).
A recent restudy of all available speci-
mens of Babinka (McAlester, 1965) has
documented the morphologic details of
the genus and has confirmed Vokes’
suggestion that Babinka shows a primi-
tive muscle pattern, although the nature
and interpretation of that pattern proved
to be more complex than had been pre-
viously suspected. Babinka was found
to have 8 pairs of pedal muscle scars
and a unique series of much smaller
scars which probably represent the site
of gill muscle attachment. The combined
pedal-gill muscle scar patternin Babinka
is almost identical to the pattern of
(433)
434 A. McALESTER
pedal and gill muscle attachmentin Neo-
pilina and in some early fossil mono-
placophorans. This close similarity
strongly suggests that the pattern in
Babinka is an inheritance from some
monoplacophora-like ancestor. The re-
study has also shown that in all features
except the pedal and gill muscle scars,
Babinka is a typical lucinoid bivalve.
Among the features which are indicative
of lucinoid affinities are the character-
istic shape, elongate anterior adductor
scar, non-sinuate pallialline, andtypical
lucinoid hinge, dentition and ligament.
Babinka is known only from lowest
Middle Ordovician rocks and is one of
the first bivalves to appear in the fossil
record. The first undoubted lucinoid
bivalves appear abruptly about one period
later, in Middle Silurian deposits, and
thus Babinka shows the proper strati-
graphic positiontohave beenanancestral
lucinoid bivalve. The stratigraphic and
morphologic evidence combine to in-
dicate that Babinka represents a tran-
sition between the large, successful,
Silurian to recent superfamily, Lucin-
acea, and some monoplacophora-like
ancestor.
Babinka provides the first direct evi-
dence of a transition between the Bi-
valvia and a more primitive ancestral
form, and the genus is therefore of
extraordinary evolutionary significance.
This paper has been prepared to call
attention to the broader evolutionary
CLP d'acte no? 5 .
. ie.
a
}
FIG. 1. Life position of recent lucinacean bivalves (modified from Allen, 1958). Nutrient-laden
water is brought into the mantle cavity through a mucus-lined anterior inhalent tube constructed
by the foot. In some genera the posterior exhalent current discharges directly into the sediment,
in others it is channeled to the surface through a retractable posterior siphon. The anterior face
of the elongate anterior adductor muscle is covered with cilia and acts as a preliminary sorting
area for incoming food particles.
ORDOVICIAN LUCINOID BIVALVE 435
implications of this unique fossil, and
to provide a preliminary revision of
the higher classification of lucinoid bi-
valves in the light of the phylogenetic
position of Babinka. The systematics
of Babinka and the detailed evidence for
its transitional evolutionary position
have been treatedelsewhere (McAlester,
1965).
HABITS AND EARLY GEOLOGIC
HISTORY OF LUCINOID BIVALVES
Allen’s functional studies of recent
Lucinacea (1958, 1960) have shown that
all members of the group share unique
adaptations for life as deeply buried
suspension feeders. Unlike most bi-
valves adapted for such a life, lucinoids
do not have a posterior siphon through
which nutrient-laden water is drawn into
the mantle cavity. Instead, the Lucin-
acea have the peculiar ability to use
the foot not only for burrowing and
locomotion, but also for the construction
of a mucus-lined, anterior inhalent tube
which connects the front edge of the
mantle cavity with the surface of the
sediment (Fig. 1). The foot is long
and cylindrical and may be extended from
3-10 times the shell height, thus per-
mitting the animal to live buried at a
considerable depth. After burial, the
animals tend to remain in one position
for long periods, but if disturbed or
uncovered, they can readily burrow into
the sediment and construct a new in-
halent tube. Various morphologic
features of the Lucinacea are corre-
lated with this specialized mode of life.
In particular, the characteristic elongate
anterior adductor muscle and anteriorly
expanded shell shape serve to facilitate
preliminary ciliary sorting of food
particles brought in by the anterior in-
halent current.
If we accept the reasonable assumption
that fossil lucinoids shared the adap-
tations for infaunal filter feeding found
in all recent Lucinacea, then the develop-
ment of these adaptations had particular
evolutionary significance because lucin-
oid bivalves appear in the geologic record
long before the first appearance of more
typical siphonate infaunal bivalves. The
first undoubted lucinoid forms appear
fully developed in Middle Silurian
deposits, whereas the first strongly
Siphonate bivalves (other than the
Specialized, deposit-feeding Nuculan-
idae) do not appear before the Carbon-
iferous, and do not become really
common until Mesozoic time. The fossil
record therefore indicates that the lucin-
oid anterior inhalent tube was an ex-
tremely early specialization for a deeply
buried suspension feeding mode of life.
Lucinoid forms appear to have been the
only major group of bivalves with adap-
tations for occupying this ecologic niche
throughout much of Paleozoic time. If
Babinka represents an ancestral lucinoid
form, then lucinoids, along with the nu-
culoids and some other problematic
groups, are among the first bivalves to
appear in the fossil record. Lucinoids
thus appear to represent a major adap-
tive branch of the Bivalvia with distinc-
tive specializations and habits that origi-
nated in the initial Paleozoic evolutionary
radiation of the Class. Like the nucu-
loids, lucinoids have survived since the
early Paleozoic and are still a diverse
and successful group in modern oceans.
PROBABLE POLYPHYLETIC
ORIGIN OF THE BIVALVIA
This extremely early evolutionary
differentiation of the Lucinacea and the
transitional evolutionary position of Bab-
inka suggest that lucinoid bivalves arose
independently from some monoplaco-
phora-like, non-bivalved ancestor. With
perhaps a single exception, there is as
yet no compelling paleontologic or
zoologic evidence to support a hypothesis
that Babinka and later lucinoid forms
are themselves ancestral to other major
groups of bivalves. Apparently the
lucinoid mode of life has persisted in-
dependently since the early Paleozoic
and has given rise to few, if any, other
major bivalve adaptations. Lucinoid
436 A. McALESTER
bivalves are probably a separate and
distinctive evolutionary branch of mol-
luscs which arose independently from a
more primitive ancestral form. This
suggests that other distinctive groups
of the Bivalvia may also have evolved
independently from non-bivalved mol-
luscan ancestors. Complete restudy of
the earliest Paleozoic fossil bivalves
will be necessary to work out the details,
but there is now enough evidence to
predict that the Bivalvia are similar to
the Mammalia and other major animal
groups in having a “polyphyletic” origin
from more primitive ancestral forms.
PRELIMINARY REVISION OF
LUCINOID HIGHER CLASSIFICATION
The independent origin and separate
development of lucinoid bivalves suggest
some major revisions in the traditional
higher classification of the group. With-
in the Bivalvia, the superfamily Lucin-
acea is usually assigned to a suborder
or order “Heterodonta”, which normally
includes such diverse groups as the
astartaceans, carditaceans, glossa-
ceans, cardiaceans, veneraceans, mac-
traceans and tellinaceans. This associ-
ation of many unlike and ‘divergently
adapted superfamilies into a larger
“heterodont” taxon has been justified
primarily on the basis of vaguely similar
patterns of dentition. The fossil record
of lucinoid bivalves, combined with
Allen’s recent discoveries concerning
the unique adaptations of the group,
indicates that the Lucinacea represent
a separate branch of the Bivalvia which
are probably unrelated to most “hetero-
dont” bivalves with which they are tra-
ditionally associated. Among the 15 or
so superfamilies normally assigned to
the “Heterodonta”, only the Leptonacea
[=Erycinacea] show morphologic and
adaptive features which clearly suggest
an evolutionary relationship to the Lucin-
acea (Popham, 1940; Morton et al.,
1957; Oldfield, 1955, 1961). The Lepton-
acea are first clearly recognizable in
the fossil record in the early Paleogene,
and they may represent a late evo-
lutionary offspring of the Lucinacea.
Continued association of the Lucinacea
with other “heterodont” superfamilies
cannot now be supported from the fossil
record nor from the morphology and
adaptations of recent forms.
Within the Lucinacea, 3 distinctive
families are universally recognized, and
an additional 4 families are sometimes
assigned to the superfamily on less con-
vincing evidence. These families and
their approximate known geologic ranges
are:
Assignment to Lucinacea certain:
Lucinidae - Silurian to recent
Thyasiridae - Cretaceous to re-
cent
Diplodontidae (=Ungulinidae)-
Cretaceous to recent
Assignment to Lucinacea question-
able:
Mactromyidae (=Unicardiidae)-
Triassic to Cretaceous
Tancrediidae - Triassic to Creta-
eous
Fimbriidae (=Corbidae) - Trias-
sic to recent
Cyrenoididae - recent only
Allen’s detailed comparative study of
recent lucinoids (1958) treated the 3
characteristic families Lucinidae, Thya-
siridae and Diplodontidae. His work
suggested that these families exhibit
an evolutionary series from the more
“primitive” Diplodontidae, through the
Thyasiridae, to the more “specialized”
Lucinidae. The Diplodontidae were con-
sidered to be primitive because they
are morphologically and adaptively the
most similar to typical heterodont, eula-
mellibranchiate bivalves, from which the
Lucinacea were presumed to have
evolved. In particular, the Diplodont-
idae show a weaker anterior inhalent
current and more complex gill pattern
than do the Lucinidae. In the Lucinidae
these features were considered to be
the result of secondary specialization.
The fossil record shows that the an-
terior inhalent current is in fact an
extremely early specialization for an
ORDOVICIAN LUCINOID BIVALVE 437
it Шут
Diplodontidae
> y
i ф | | - Ze ES
)
CAEN AO © LEE
Cretaceous
Jurassic
М Е ОДО iC
Lucinidae
Triassic
Carb-Perm.
LUCINACEA
Ordovician
ancestral mollusc
Cambrian
FIG. 2. Proposed evolutionary relations of Babinkacea, Lucinacea and Leptonacea. The width
of the shaded areas is approximately proportional to the generic diversity of the taxa.
438 A. McALESTER
infaunal suspension feeding mode of life
and is not a secondary specialization
from some more “typical” bivalve
pattern. This suggests that Allen’s
inferred evolutionary series of the 3
families is actually reversed, and that
the similarities between the “primitive”
Diplodontidae and typical “heterodont”
bivalves is the result of convergent
evolution from basically different ances-
tral forms. This possibility is further
suggested by the late geological appear-
ance of representatives ofthe Diplodont-
idae and Thyasiridae, both of which are
unknown before the Cretaceous (Fig. 2).
The independent evolutionary develop-
ment of lucinoid bivalves suggests that
the entire group should be assigned to
a separate bivalve taxon of the highest
rank. The Leptonacea have most
probably evolved from the Lucinacea
and can reasonably be assigned to the
same higher taxon. There now appears
to be no sound phylogenetic basis for
associating other major bivalve groups
with the lucinoids and leptonoids.
Babinka is most closely related to the
Lucinacea, but its unique evolutionary
position can best be represented by
assignment to a separate superfamily
under a larger sub-taxon which also
includes the Lucinacea. Within the
Lucinacea, the Lucinidae probably
represent the ancestral stock from which
the other familiesarose. These relation-
ships are shown in Fig. 2. Additional
anatomical and morphological data will
be necessary before the families Mactro-
myidae, Tancrediidae, Fimbriidae and
Cyrenoididae can be unequivocally
assigned to the Lucinacea.
These suggestions are summarized in
the following tentative scheme of lucin-
oid higher classification. To avoid
nomenclatural conflicts with the forth-
coming bivalve volume of the “Treatise
on Invertebrate Paleontology”, noformal
names are given to those higher cate-
gories which are suggested here for
the first time.
LUCINOID SUBCLASS OR ORDER
Lucinid Order or Suborder
Superfamily Babinkacea
Family Babinkidae
Superfamily Lucinacea
Family Lucinidae
Family Thyasiridae
Family Diplodontidae
[? Family Mactromyidae]
[? Family Tancrediidae]
[? Family Fimbriidae]
[? Family Cyrenoididae]
Leptonid Order or Suborder
Superfamily Leptonacea
[Families omitted]
ACKNOWLEDGMENTS
I am most grateful to Drs. Copeland
MacClintock, N. D. Newell and J. H.
Ostrom for reading the manuscript and
offering many helpful suggestions, and
to Miss Martha Dimock for preparing
the text figures. The restudy of Babinka
which led to these conclusions was
supported in part by grant No. G19961
from the National Science Foundation,
and in part by the Charles Schuchert
Fund of the Peabody Museum, Yale
University.
REFERENCES
ALLEN, J. A., 1958, On the basic
form and adaptations to habitat in the
Lucinacea (Eulamellibranchia). Phil.
Trans. Roy. Soc. London, B, 241:
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‚ 1960, The ligament of the
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COX, L. R., 1959, The geological his-
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ORDOVICIAN LUCINOID BIVALVE 439
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‚1960, Thoughts on the classi-
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HORNY, R., 1960, On the phylogeny
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MERKLIN, R. L., 1962, Ob odnoy novoy
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OLDFIELD, E., 1955, Observations on
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, 1961, The functional morpho-
logy of Kellia suborbicularis (Monta-
gu), Montacuta ferruginosa (Montagu)
and M. substriata (Montagu), (Mol-
lusca, Lamellibranchiata). Proc. ma-
lacol. Soc. London, 34: 255-295.
POPHAM, M. L., 1940, The mantle
cavity of some of the Erycinidae,
Montacutidae and Galeommatidae with
special reference to the ciliary mech-
anisms. J. marine Biol. Ass. U. K.
24: 549-587.
RUZICKA, B. & PRANTL, F., 1960,
Types of some Barrande’s pelecy-
pods (Barrandian). Zvlästni Otisk
Casopisu Narodniho Musea, oddil pri-
rodovedny, (1): 48-55. [in Czech with
English Summary].
VOGEL, K., 1962, Muscheln mit Schlos-
szähnen aus dem spanischen Kam-
brium und ihre Bedeutung fiir die
Evolution der Lamellibranchiaten.
Akad. Wiss. Mainz, Abh. math.-
naturw. Kl., Jg. 1962, no. 4, 52p, 5 pls.
VOKES, H. E., 1954, Some primitive
fossil pelecypods and their possible
significance. J. Washington Acad.
Sci. 44: 233-236.
RESUMEN
IMPLICACIONES SISTEMATICAS Y EVOLUTIVAS DE UN BIVALVO
TRANSICIONAL LUCINOIDE DEL ORDOVICIANO
Evidencia morfolögica y estratigräfica indica que el raro bivalvo del Ordoviciano
Babinkia es una transición evolutiva entre la superfamilia Lucinacea y algunos
moluscos ancestrales de tipo monoplacöforo.
Evidencia paleontolögica, y estudios
comparativos funcionales de formas recientes, sugieren que los Lucinacea, Lepton-
acea y Babinkia representan un linaje evolutivo independiente que ha mantenido
caracteres adaptivos únicos desde el Paleozoico antiguo. Este linaje probablemente
deberá ser tratado como un taxon separado, de bivalvos de alta categoria. Los
Lucinoidea no parecen haber dado origen a otros grupos mayores de bivalvos y
probablemente no estan relacionados a la mayoría de otras formas “heterodontas”
con las cuales se asociaban comunmente.
El origen independiente de los lucinoideos
sugiere que la clase Bivalvia tuvo un origen polifilético de otros moluscos ancestrales
no bivalvos.
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INDEX TO SCIENTIFIC NAMES
Abatus, 187
cavernosus, 187
Acer, 45
rubrum, 45
Achnanthes, 68
exigna heterovalvata, 68
lanceolata, 68
minutissima, 68
minutissima cryptocephala, 68
Achasmea, 184, 185
thalassemicola, 185
acicularis, Nitzschia, 69
Acleioprocta, 264, 279, 372
Aclididae, 171
Acmaea, 381
Acochlidiacea, 357, 365, 366, 369, 371
Acoela, 327, 330, 334, 345, 346, 353,
354, 364, 371
acuta, Physa, 311
acuta, Pleurocera, 1-80
acutissima, Eulima, 134, 135
acutum tractum, Pleurocera, 10
Acteocina, 364, 371
exima, 364
Acteon, 334, 336-339, 344, 345, 353,
361, 371
punctocaelatus, 336, 337, 338
tornatilis, 337, 338
Acteonidae, 345, 346, 354, 364, 366,
368, 369, 370, 371
actinariophila, Nipponomontacuta, 184
aeglefinis, Melanogrammus, 198
Aeolidia, 345, 351
papillosa, 345, 351
Aeolidiacea, 349, 351, 366, 372
aequicostatus, Heterocyathus, 185
aestivalis, Vites, 45
aestuariorum, Portlandia,
affinis, Cadlina, 348
affinis, Cymbella, 68
affinis, Herviella, 251
affinis, Upogebia, 189
Aglaja, 263, 264, 334, 361, 364
splendida, 263, 264
Aglajidae, 263, 265, 344, 357, 360, 361,
364, 366, 371
205
Aglossa,
Akera, 186, 364
bullata, 186, 364
nana, 186
Akeratidae,
akkeshiensis, Ercolania,
171, 172
364, 366, 368, 369
269
441
akkeshiensis, Stiliger, 269
alba, Balcis, 151, 163, 169
alba, Philine, 359, 361, 364
alba, Quercus, 45
albida, Doto, 264, 279
albopunctata, Dendrodoris, 335, 345
Alderia, 353, 354, 355, 356, 357, 370
modesta, 354
Aligena, 184, 186
elevata, 186
Amauropsis, 203
islandica, 203
ambigua, Brachystomia, 365
ambrigua, Melosira, 68
amboinensis, Cycladoconcha, 188
Ambloplites, 10
rupestris, 10
americana, Vallisneria, 45
americanus, Scirpus, 45
amoena, Chromodoris, 247, 248
Amnicola, 42, 43, 103, 107-109
hendersoni, 109
idahoensis, 109
limosa, 42, 43
longinqua, 104, 108
micra, 104, 108
micrococcus, 103, 109
pilsbryana, 104, 108
pilsbryi, 108
Amphibia, 323
Amphibola, 367
Amphineura, 186
Amphipleura, 69
pellucida, 69
Amphiura, 188
filiformis, 188
Amphora, 68
normani, 68
Ampullariidae, 419
Anabaena, 14, 45
Analogium, 250
236, 265, 327, 334, 337, 345,
352-354, 363-370
anceps, Helisoma, 42
Anaspidea,
anceps, Stauroneis, 67, 69
Anculosa, 9, 36, 38, 53, 58, 60
carinata, 36, 53, 58
subglobosa, 36
Ancylus, 400
fluviatilis, 400
Angitrema, 9
verrucosa, 9
442 MALACOLOGIA
angusta, Cyrtodaria, 202, 203
Anisodoris, 338
nobilis, 338
Annelida, 184, 186
Anodonta, 42
grandis, 42
Anomoeoneis, 67
sphaerophora, 67
Anthenoides, 116
rugulosus, 116
anthonyi, Eurycaelon, 36
Antiopella, 351
muloc, 351
aperta, Haminoea, 243
aperta, Philine, 359, 361, 362, 364
Aphrodite, 186, 189
Aplodinotus, 69
grunniens, 10
Aplysia, 212, 263, 265, 266, 334, 338-
343, 352, 353, 364, 420
dactylomela, 263, 265
juliana, 212
parvula, 263, 266
parvula nigrocincta, 266
pulmonica, 263, 266
punctata, 364
Aplysiidae, 236, 263, 265, 364, 366
Aplysiinae, 263, 265
Aporrhais, 185
appressa, Mesodon, 311
appressa, Polygyra, 311
avachnoidea, Goniobasis, 36
arborescens, Doridopsis, 250
Archidoris, 365
tuburculata, 365
arctica, Hiatella, 203
arctica, Portlandia, 400
arctica, Yoldia, 400
arenarius, Murex fulvescens, 229
Armina, 350, 351
Arminacea, 349, 351, 366, 372
arrhynchus, Megadenus, 116, 129, 134,
151, 172, 173, 174, 175
Arthropoda, 184, 189
Aspidobranchia, 114
Aspidosiphon, 185
Asteroidea, 115
Asteronotinae, 264, 276
Asterophila, 111-181
japonica, 111-181
Asterophilidae, 112, 114, 175
atra, Holothuria, 212
atromarginata, Casella, 264, 273
Atyidae, 236, 327, 357-359, 364, 366,
370, 371
auricularia, Dolabella, 263, 266
Auristomia, 185
perezi, 185
aurita, Cercaria, 69
australis, Scioberetia, 187
Australorbis, 81, 95.
glabratus, 81, 95
avara, Catinella, 310
avara, Succinea, 310
Axius, 184, 189
plectorhychus, 189
Babinka, 419-425
Babinkacea, 423, 424
Babinkidae, 424
Baeolidia, 282
Balcis, 151, 163, 169, 175
alba, 151, 163, 169
devians, 151, 163, 169
balfouriana, Diatomella, 67
banyluensis, Dondice, 351
Barnea, 187
candida, 187
barronensis, Goniobasis livescens, 55
Basommatophora, 236, 311, 368, 379
Bathydoris, 348
Batrachospermum, 45, 68
vugum, 45, 68
bayeri, Elysia, 263, 264, 270, 271
Bedeva, 229
hanleyi, 229
Bellevalia, 323
Berghia, 282, 351
coerulescens, 351
Berthella, 264, 271, 347, 348
grisea, 264, 271
Berthelinia 264, 271, 334, 347-357
citrina, 264, 271
Betula, 45
papyrifera, 45
bicolor, Gymnodoris, 236, 249, 250
bicolor, Trevelyana, 249
bidentata, Mysella, 183, 185, 186, 187
188, 189
bifida, Hermaea, 356
Bilateria, 331
binotata, Haminoea, 240
binotata japonica, Haminoea, 240
Biomphalaria, 379-398
pfeifferi, 379-398
INDEX, VOL. Ш
Bivalvia, 183, 186, 197, 419-425
blakei, Deima, 116
Blepharipoda, 189
occidentalis, 189
bodanica, Cyclotella, 68
boeckii, Brebissonia, 67
boholiensis, Discodoris, 276
Bornella, 264, 279
digitata, 264, 279
Bornellidae, 264, 279
Bosellia, 353, 356
mimetica, 353
Bourvieria, 347, 348
ocellata, 348
brachiata, Ophiocnida, 188
Brachidontes, 186
granulatus, 186
multiformis, 186
Brachystomia, 365
ambigua, 365
Brebissonia, 67
boeckii, 67
brevis, Io fluvialis, 35
brevistriata, Fragilaria, 68
briareus, Ennoia, 280
briqua, Chromodoris, 236, 245-249
Brissopsis, 187
lyrifera, 187
brunelli, Sphaerumbonella, 184
Bryozoa, 184, 185
Buccinacea, 230, 231
Buccinum, 8
virginicum, 8
Bulinus, 380
Bulla, 360, 364, 370, 371
gouldiana, 360, 364
Bullacea, 236, 263, 265
bullata, Akera, 186, 364
Bullidae, 327, 357, 358, 364, 366, 370,
371
Busycon, 228
bylgia, Catriona, 280
Cadlina, 276, 348
affinis, 348
Cadlinella, 247
Cadlinellinae, 247
Cadulus, 203
Caecum, 203
californica, Cerithidea, 22
californica, Hancockia, 350
californianus, Mytilus, 186
californiensis, Fontelicella, 103-109
Caliphylla, 354, 355, 356, 370
mediterranea, 356
Callianassa, 189
major, 189
Calliostoma, 185
conuloides, 185
callosa, Haminoea, 241
Calma, 351, 372
Caloria, 253
calyculata, Smaragdinella, 236, 237,
238
camdenensis, Cyrtodaria, 202, 203, 204
Campeloma, 42, 43
decisum, 42, 43
campestris, Succinea, 310
campestris vagans, Succinea, 310
canadensis, Elodea, 45
canaliculata, Pleurocera, 9, 36, 58, 63
canaliculatum undulatum, Pleurocera,
9, 18, 21, 22, 25, 30-40
candida, Barnea, 187
capitata, Limapontia, 365
capucina, Fragilaria, 68
Capulidae, 159, 171
caputserpentis, Cypraea, 212
Carcinides, 189
maenas, 189
Carex, 45
carinata, Nitocris, 36, 53, 58
carpenteri, Triopha, 333, 345
Carya, 45
tomentosa, 45
Casella, 264, 273
atromarginata, 264, 273
rufomarginata, 264, 273
Catinella, 309-325
avara, 310
rotundata, 309, 310, 313, 321
texana, 309, 310, 321
vagans, 310
vermeta, 309-325
Catriona, 263, 264, 274-280
bylgia, 280
cucullata, 280
lonca, 263, 264, 274-280
maua, 279
susa, 280
urquisa, 263, 264, 274-280
caudata, Eupleura, 185
Caulerpa, 266
cavernosus, Abatus, 187
Cavolinidae, 365
443
444 MALACOLOGIA
Cerastoderma, 189
edule, 189
Ceratobornia,
longipes, 186
cedrosensis, Fontelicella, 108
cedrosensis, Paludestrina, 104, 108
celebensis, Stilifer, 135, 138, 151, 172
celtica, Onchidella, 254
Cephalaspidea, 236, 263, 265, 352, 357,
363-370
184, 186, 189
Cerberilla, 253
Ceratophyllum, 45
demersum, 45
Cercaria, 69, 70, 71
aurita, 69, 70
gorgonocephala, 69, 70
sagittavia, 1
Cerithidea, 22
californica, 22
Cerithium, 22
vulgatum, 22
Chama, 186
Chara, 45
vulgaris, 45
Chelidonura, 263, 265
hirundinina, 263, 265
inornata, 263, 265
Chlorella, 67
variegatus, 67
christenseni, Montacuta, 187
Chromodoridinae, 236, 247, 248, 264,
272
236, 244-249, 264, 272,
273
Chromodoris,
alderi, 248, 249
amoena, 247, 248
aureopurpurea, 248
briqua, 236, 245-249
crossei, 273
fidelis, 236, 244-246
flammulata, 245
hilaris, 248
tnornata, 248
juvenca, 248
lactea, 245
lata, 245
lineata, 248, 249
lineolata, 264, 272
quadricolor, 249
reticulata, 248
vuncinata, 248
venusta, 264, 272
Cidaris, 187
cidaris, 187
cidaris, Cidaris, 187
Cincinnatia, 103, 107, 108
integra, 103, 107
cincinnatiensis, Pomatiopsis,
cinerea, Urosalpinx, 226
Cirripedia, 113
cistula, Cymbella, 67
cistula, Lasaea, 186
citrina, Berthelinia,
claror, Herviella,
Clavagella, 183
clavaeformis, Goniobasis,
clarkiae, Lepton, 185, 186
clarkiae, Potidoma, 185
Clione, 362
Clionopsis, 362, 365
grandis, 365
Cleopatra, 22
Cliopsidae, 365
Cleioprocta, 236, 280, 282
Clonorchis, 3
sinensis, 3
clausa, Natica, 203
Clymenella, 186
torquata, 186
coccinea, Quercus, 45
Cocconeis, 68
pediculus, 68
placentula, 68
cochleariformis, Sacculosiphonaria, 257
cochleariformis, Siphonaria, 257
Coelenterata, 184
coerulescens, Berghia, 351
coivala, Hermaea, 356
Colobocephalus, 369
comalensis, Goniobasis, 53
comis, Janolus, 351
communis, Dendrodoris, 250
communis, Turritella, 185
compressa, Pseudopythina, 189
concharum, Jousseaumiella, 185
conspicuus, Ischnochiton, 186
constrictum, Gomphonema, 68
construens, Fragilaria, 68
construens subsalina, Fragilaria, 68
conuloides, Calliostoma, 185
conuloides, Zizyphinus, 185
copallina, Rhus, 45
Copepoda, 113
corallinaceus, Vermetus, 186
29, 82, 99
264, 271
235, 251-253
36, 58
INDEX, VOL. III
coralliophila, Thyreopsis, 184
Corbidae, 422
cordatum, Echinocardium, 187
Cornus, 45
stolonifera, 45
cornuta, Langerhansia, 185
correcta, Goniobasis livescens, 9, 36,
38, 53, 55, 56, 70
Coryphellina, 351
Coscinodiscus, 68
lacustris, 68
Costasiella, 267
ocellifera, 267
nonatoi, 267
costellatum, Isognomon, 225
Cotylogaster, 69, 70, 71
occidentalis, 69, 70, 71
crassicornis, Hermissenda, 336-338,
345
Cratena, 253, 280, 283
Creseis, 333, 365
virgula, 333, 365
cribosa, Dendrophyllia, 185
Cribrella, 115
crispata, Tridachia, 356
crispatus, Ctenodiscus, 115
crocata, Haminoea, 240, 241
crossei, Chromodoris, 273
crossei, Hypselodoris, 273
crosslandi, Patinapta, 188
cruenta, Platydoris, 264, 277
Cryptobranchia, 236, 264, 271
cryptocephala, Achnanthes minutissima,
68
cryptocephala, Mastogloia smithü, 69
cryptocephala, Navicula, 69
cryptocephala veneta, Navicula, 69
cucullata, Catriona, 280
cucumariae, Diacolax, 127
cuenoti, Erycina, 185
cuis, Hypselodoris, 263, 269, 272, 273
cuneata, Pythinella, 185
cuneata, Rochelfortia, 185
curiosa, Holothuria, 188
curiosa, Noumeaella, 282
curtatum, Pleurocera unciale, 36
curtum, Pleurocera, 36
Cuthonidae, 264, 279
Ctenodiscus, 115
crispatus, 115
Ctenosculidae, 171
Ctenosculum, 114
445
hawatiense, 114
Cycladella, 184
Cycladoconcha, 184, 188
amboinensis, 188
Cyclope, 221, 229
neritea, 221, 229
Cyclotella, 68
bodanica, 68
Cyerce, 264, 269
nigra, 264, 269
Cylichna, 334, 361, 364, 371
cylindracea, 364
Cylichnella, 371
cylindracea, Cylichna, 364
Cylindrobulla, 334, 341, 352, 353, 357,
369, 370
Cylindrobullidae,
Cylindrocapsa, 67
geminella, 67
cymbalum, Lamprohaminoea,
327, 366
236, 242-
244
Cymbella, 67
cistula, 67
cymbiformis, 68
delicatula, 68
lanceolata, 67
naviculiformis, 68
prostrata, 68
ventricosa, 68
cymbiformis, Cymbella, 68
Cymbulia, 420, 428
Cypraea, 212
caputserpentis, 212
Cyrenoididae, 422, 424
Cyrtodaria, 197-210
angusta, 202, 203
camdenensis, 202, 203, 204
jenisseae, 202, 203, 204
kurriana, 197-205
neuvillei, 202, 203
siliqua, 197-210
transcaspica, 202, 203
vagina, 203
cysticola, Megadenus, 151
dactylomela, Aplysia, 263, 265
dactylomela, Verria, 263, 265
Decapoda, 189
decisum, Campeloma, 42, 43
decorata, Hallaxa, 264, 273
Deima, 116
blakei, 116
deimatis, Gasterosiphon, 116, 127, 146
446 MALACOLOGIA
delicatula, Cymbella, 68 erubescens, 276
deltaura, Upogebia, 189 indecora, 275
demersum, Ceratophyllum, 45 labifera, 276
dendritica, Hermaea, 356 liturata, 275
Dendrodoris, 236, 250, 251, 264, 277, lora, 263, 268, 269, 273-275
335, 336, 345 lutescens, 276
albopunctata, 335, 345 pallida, 275, 276
communis, 250 palma, 276
erubescens, 236, 250, 251 voniheringi, 349
melaena, 250 ylva, 263, 274-276
nigra, 236, 250, 264, 277 Divariscintilla, 184, 189
rubra, 250 maoria, 189
Dendrodorididae, 236, 264, 277 Dolabella, 263, 266, 353
Dendronotacea, 349, 351, 365, 366, 372 auricularia, 263, 266
Dendronotoidea, 264, 279, 365 scapula, 266
Dendronotus, 351, 365, 372 Dolabellinae, 263, 266
frondosus, 351, 365 Dolabrifera, 236, 244, 263, 266
Dendrophyllia, 185 dolabrifera, 236, 244, 263, 266
cribosa, 185 maillardi, 244
dendyi, Trochodota, 188 nicaraguana, 244
Dentalium, 203 variegata, 244
deshayesiana, Mylitta, 189 dolabrifera, Dolabrifera, 236, 244, 263,
deshayesii, Kellia, 185 266
Desmidium, 67 Dolabriferinae, 236, 263
grevillii, 67 donacina, Montacuta, 188
devians, Balcis, 151, 163, 169 Dondice, 253, 351
Devonia, 184, 188 banyluensis, 351
ohshimai, 188 Doridacea, 344, 349, 365, 366, 372
perrieri, 188 Dorididae, 236, 264, 272, 365
Diacolax, 127, 175 Doridoidea, 236, 264, 271
cucumariae, 127 Doridopsis, 250
Diaphana, 364 arborescens, 250
minuta, 364 erubescens, 250
Diaphanidae, 327, 352, 353, 357-371 nigra, 250
diardii, Hypselodoris, 273 nigra luteopunctata, 250
Diatomella, 67 Doriopsila, 335
balfouriana, 67 Doris, 245, 249, 250
dicoelobius, Paedophoropus, 138, 151, fidelis, 245
168, 172 magnifica, 249
Dictyosphaerium, 67 nigra, 250
pulchellum, 67 preciosa, 245
digitata, Libidoplax, 188 Doto, 264, 279, 350, 351
digitata, Bornella, 264, 279 albida, 264, 279
dilatatus, Elliptio, 42, 43 uva, 351
Diplodontidae, 422, 424 Dotoidae, 264, 279
dissimilis, Mudalia, 35 Drupa, 211-233
Discodorinae, 264, 273 vicina, 211-233
Discodoris, 263, 268, 269, 273-276, 349 dubia, Discodoris, 275
boholiensis, 276 dufourei, Melanopsis, 22
dubia, 275 Dysnomia, 42
egena, 275 triquetra, 42
erythraeensis, 275 eburnea, Mucronalia, 129
INDEX, VOL. II
Echinarachnius, 200, 201
parma, 200, 201
echinocardiophila, Montacuta, 187
Echinocardium, 187
cordatum, 187
flavescens, 187
Echinodermata, 184, 187
Echinoidea, 187
Echinus, 187
esculentus, 187
Echiuroidea, 184, 185
edule, Cerastoderma, 189
edulis, Mytilus, 189
egena, Discodoris, 275
Eledone, 288, 303
cirrosa, 288, 303
elegans, Halgerda, 264, 276
elegans, Haminoea, 244
elevata, Aligena, 186
Elimia, 9
Elliptio, 42, 43
dilatatus, 42, 43
Elodea, 45
canadensis, 45
elongatum, Phascolosoma, 185
Elysia, 263-271, 353, 356, 364, 365,
370
bayeri, 263, 264, 270, 271
‘hedgpethi, 365
latipes, 271
livida, 270
marginata,
ornata, 270
тата, 263, 264, 268-271
264, 270
thysanopoda, 264, 270
viridis, 356
Elysiacea, 264, 267, 365
Elysiidae, 264, 270, 365, 366
emarginata, Stagnicola, 311
Embletonia, 351, 345, 372
fuscata, 351
pallida, 351
emeryensis, Goniobasis, 46
Ennoia, 280, 283
briareus, 280
longicirrha, 283
Enteroxenos, 117, 133, 156, 175
Entocolax,
170-175
ludwigi, 117, 143
rimsky-korsakovi,
schiemenzi, 117
143, 170, 174
117, 132, 143, 151, 159-163,
schwanwitschi,
trochodotae, 117, 151, 159
Entoconcha, 117, 159, 175
mirabilis, 117
Entoconchidae, 112-181
Entomotaeniata, 365
Entovalva, 184, 188
major, 188
mirabilis, 188
ohshimai, 188
perrieri, 188
semperi, 188
Eolidacea, 282
151, 159-163, 170
Eolidoidea, 236, 264, 279
Ephippodonta, 184, 185, 189
lunata, 184, 189
macdougalli, 184, 189
muvakamii, 184
turnbullae, 184, 189
Epithemia, 67, 68
turgida, 67
zebra, 68
equestris, Eulima, 135
equestris, Melanella, 151
Ercolania, 264, 267-269
akkeshiensis, 269
illus, 264, 267, 269
noto, 269
pancerii, 267
trinchesei, 269
erinaceus, Murex, 231
erubescens, Dendrodoris,
erubescens, Discodoris, 276
erubescens, Doridopsis, 250
Erycina, 185
cuenoli,, 185
Erycinacea, 183-195, 422
erythraeensis, Discodoris, 275
esculentus, Echinus, 187
Eubranchus, 372
Eudoridacea, 236
Eulima, 134, 135
acutissima, 134, 135
equestris, 135
Eulimidae, 127
Eunereis, 186
longissima, 186
Eupleura, 185
caudata, 185
Eupomotis, 10
gibbosus, 10
Eurycaelon, 9, 36
236, 250, 251
448
anthonyi, 36
Euthyneura, 263, 320, 343, 366, 367,
| - 371
exigua, Herviella, 251
exigua heterovalvata, Achnanthes, 68
exigua, Navicula, 69
exima, Acteocina, 364
evelinae, Miesea, 279, 351
evelinae, Muessa, 263, 264, 280-283
evelinae, Onchidella, 235, 253, 255, 256
Facalaninae, 253
Facelinidae, 253, 282, 283
fasciata, Ulva, 212
Favorinidae, 236, 253, 263, 264, 270,
282, 283
Favorininae, 236, 253, 264, 270, 282,
283
fenestra, Tabellaria, 67, 68
Ferrissia, 60
shimekii, 60
ferruginea, Limanda, 198
ferruginosa, Montacuta, 187
fidelis, Chromodoris, 236, 244-246
fidelis, Doris, 245
fidelis, Glossodoris,
filiformis, Amphiura,
Fimbriidae, 422, 424
flammulata, Chromodoris,
flammulata, Platydoris,
flavescens, Echinocardium,
flavescens, Onchidella, 256
flexilis, Nitella, 45
floccosa, Microspora, 67
fluvialis, Io, 22, 26, 34, 58, 73
fluvialis brevis, Io, 35
fluvialis lyttonensis, Io, 35
245
188
245
264, 277
187
fluviatilis, Ancylus, 400
Fontelicella, 103-110
californiensis, 103-109
cedrosensis, 108
hendersoni, 104-109
idahoensis, 107-109
intermedia, 108
longinqua, 108
micrococcus, 109
pilsbryana, 108
robusta, 109,
stearnsiana, 107, 108
truckeensis, 108
fontinalis, Salvelinus, 11
Forcipulata, 115
formosana, Oncomelania, 81-102
MALACOLOGIA
Fragilaria, 68
brevistriata, 68
capucina, 68
construens, 68
construens subsalina, 68
frigida, Yoldiella, 203
frondosus, Dendronotus,
Fronsella, 184, 185
ohshimai, 185
Fryeria, 264, 279
rüppelli, 264, 279
fulvescens arenarius, Murex, 229
funebris, Kentrodoris, 264, 276
furcigerum, Staurastrum, 67
fuscata, Embletonia, 351
fuscus, Laevapex, 42, 43
fuscocineria, Mertensiothuria,
Gadus, 198
morhua, 198
galba, Haminoea,
Galeomma, 184
Gasterosiphon,
351, 365
188
241
116, 127, 138, 145, 146,
151, 173, 175
116, 127, 146
81, 113, 134, 140, 143, 146,
186, 235
Gastropteridae, 357, 360, 362, 366, 371
Gastropteron, 361
geminella, Cylindrocapsa, 67
gemmata, Mylitta, 189
gibba, Rhopalodia, 67, 68
gibbosus, Eupomotis, 10
glabra, Litigiella, 185
glabra, Montacuta, 185
glabratus, Australorbis,
glauca, Smaragdinella,
Globiferina, 283
noumeae, 283
globulosa, Hydromyles, 362
Glossodoris, 245, 248, 272, 273
fidelis, 245
hilaris, 248
obscura, 273
Golfingia, 185
vulgare, 185
Gomphonema, 67, 68
constrictum, 68
subtile, 68
vibrio, 67
Goniobasis, 1-80
avachnoidea, 36
clavaeformis, 36, 58
deimatis,
Gastropoda,
81, 95
236, 238
INDEX, VOL. Ш 449
comalensis, 53
emeryensis, 46
laqueata, 9, 36, 38, 40, 58
livescens, 1-80
livescens barronensis, 53
livescens correcta, 9, 38, 53, 55, 56,
70
livescens michiganensis, 53
multicarinata, 10
mutabilis, 36
proxima, 36
pulchella, 70
virginicum, 8, 35, 36, 51, 53, 58
gorgonocephala, Cercaria, 69
gouldiana, Bulla, 360, 364
gracilis, Navicula, 67
grandis, Anodonta, 42
grandis, Cliopsis, 365
granifera, Thiara, 3
granulata, Morula, 211-233
gvanulatus, Brachidontes, 186
grevillii, Desmidium, 67
grisea, Berthella, 264, 271
groenlandica, Leptasterias, 115
grunniens, Aplodinotus, “0
guamensis, Sacculosiphonaria, 236,
256, 257
guamensis, Siphonaria, 236, 255-257
Gymnodorididae, 236, 264, 277
Gymnodoris, 236, 249, 250
bicolor, 236, 249, 250
maculata, 250
Gymnosomata, 358, 362, 363, 365, 366,
368, 369
gyrina, Physa, 42, 43
Gyrosigma, 67, 69
kútzingii, 67, 69
Gyrotoma, 9, 38
Halgerda, 264, 276
elegans, 264, 276
Halimeda, 266, 270
Haliotis, 380, 381
Hallaxa, 264, 273
decorata, 264, 273
Haloa, 240
Haminoea, 235-243, 331, 358, 364, 369,
370
aperta, 243
binotata, 240
binotata japonica, 240
callosa, 241
crocata, 240, 241
elegans, 244
galba, 241
linda, 235, 236, 241-244
musetta, 235, 236, 239, 241
navicula, 364
nigro punctata, 240
ovalis, 243
rotundata, 243
simillima, 241
solitaria, 364
vitrea, 243
hamva, Pleurobranchaea, 348
Hancockia, 350
californica, 350
hanleyi, Bedeva, 229
hantzschiana, Nitzschia, 69
Harmothoé, 189
lunulata, 189
hawaiiense, Ctenosculum, 114
heathiana, Ischnochiton, 186
hedgpethi, Elysia, 365
Hedylopsidae, 357, 365
Hedylopsis, 365
suecica, 365
Helioperca, 10
incisor, 10
Heliopora, 267, 275, 277, 278
Helisoma, 11, 42
anceps, 42
trivolvis, 11, 42, 43
Helix, 311, 386, 420, 428
pomatia, 311, 420
Hemiaster, 187
hendersoni, Amnicola, 109
hendersoni, Fontelicella, 104-106
Hermaea, 356
bifida, 356
coivala, 356
dendritica, 356
Hermaeina, 336, 353, 356, 365, 370
smithi, 336, 353, 365
Hermissenda, 336-338, 345
crassicornis, 336-338, 345
Herviella, 235, 251-253, 263, 283
affinis, 251
claror, 235, 251-253
exigua, 251
mietta, 235, 252, 253
yatsui, 251, 253, 283
heterocyathi, Jousseaumiella, 185
Heterocyathus, 185
aequicostatus, 185
450 MALACOLOGIA
Heterodonta, 442
heterophylla, Populus, 45
Heteropsammia, 185
michelini, 185
heteropsammiae, Jousseaumiella, 185
heterovalvata, Achnanthes exigua, 68
Hexabranchidae, 264, 271
Hexabranchus, 264, 271
marginatus, 264, 271
Hiatella, 203
arctica, 203
Hiatellidae, 197, 198
hilaris, Glossodoris, 248
hilaris, Hypselodoris, 236, 246, 248,
249, 273
Hippoglossoides, 198
platessoides, 198
hirasei, Succinea, 311, 321
hirsuta, Trichomya, 186
hirundinina, Chelidonura,
Holothuria, 188,212 |
atra, 212
curiosa, 188
holothuricola, Megadenus,
Holothuroidea, 187
263, 265
hombergi, Tritonia, 345, 365
Hormomya, 186
multiformis, 186
horticola, Succinea, 311, 321
hupensis, Oncomelania, 82, 97, 98
huroni, Plagioporus sinitsini, 70
hyalinum, Phyllodesmium, 264, 280,
283
Hydatina, 346
Hydatinidae, 327, 345, 346, 366, 371
Hydrobia, 104, 105
truckeensis, 104
Hydrobiidae, 81, 103-106
Hydrobiinae, 103
Hydromyles, 362, 368
globulosa, 362
Hypselodoris, 236, 246-249, 263, 268,
272, 273
crossei, 273
cuis, 263, 269, 272, 273
diardii, 273
hilaris, 236, 246-249, 273
marenzelleri, 273
nigrostriata, 273
vansoni, 273
runcinata, 273
semperi, 273
tenuilinearis, 273
134, 143, 173
idahoensis, Amnicola, 109
idahoensis, Fontelicella, 107, 109
illus, Stiliger, 263, 264, 267-269
Io, 22, 26, 34, 35, 38, 73
fluvialis, 22, 26, 34, 58, 73
fluvialis brevis, 35
fluvialis lyttonensis, 35
Illex, 288, 303
illecebrosus, 288, 303
illus, Ercolania, 264, 267-269
indecora, Discodoris, 275
incisor, Helioperca, 70
incisum, Isognomon, 225
inhaerens, Leptosynapta, 188
inornata, Chelidonura, 263, 265
integra, Physa, 42, 43, 429
intermedia, Fontelicella, 108
intermedia, Pomatiopsis, 104, 108
iris, Micromya, 42, 43
Ischnochiton, 186
conspicuus, 186
heathiana, 186
magdalenensis, 186
islandica, Amauropsis, 203
Isognomon, 225, 226
costellatum, 225
incisum, 225
Janolus, 351
comis, 351
japonica, Asterophila, 111-181
japonica, Haminoea binotata, 240
japonicum, Schistosoma, 81
jenisseae, Cyrtodaria, 202-204.
Jousseaumia, 185
Jousseaumiella, 184
concharum, 185
heterocyathi, 185
heteropsammiae, 185
Juliacea, 366
juliana, Aplysia, 212
Juliidae, 355, 370
juvenca, Chroonodoris, 248
Kellia, 184-186, 189
deshayesii, 185
laperousii, 186
rubra, 185, 186
Kentrodoris, 264, 276
funebris, 264, 276
kurriana, Cyrtodaria,
kiitzingii, Gyrosigma,
kwansae, Succinea,
Labidoplax, 188
digitata, 188
197-205
67, 69
311/381
INDEX, VOL. III 451
labifera, Discodoris, 276
lactea, Chromodoris, 245
lacustris, Coscinodiscus, 68
lacustris, Navicula, 69
Laevapex, 42, 43
fuscus, 42, 43
laevis, Patinapta, 188
Lamprohaminoea, 236, 242-244
cymbalum, 236, 242-244
Lampsilis, 42, 43, 70
luteola, 10
siliquoidea, 42, 43
Lamellariidae, 114
lanceolata, Achnanthes, 68
lanceolata, Cymbella, 67
Langerhansia, 185
cornuta, 185
laperousii, Kellia, 186
lapillus, Nucella, 229, 231
laqueata, Goniobasis, 9, 36, 38, 40, 58
Lasaea, 184, 186, 187
cistula, 186
miliaris, 186
vubra, 187
scalaris, 186
subviridis, 186
lata, Chromodoris, 245
lata, Pinnularia, 69
Lathophthalmus, 236, 238, 239
smaragdinus, 236, 238
latifolia, Sagittaria, 45
latifolia, Typha, 45
latipes, Elysia, 271
Lebistes, 14
reticulatus, 14
Leersia, 45
Lehmannia, 311
marginata, 311
Leptasterias, 115, 116
polaris, 115
groenlandica, 115
Lepton, 184-189
clarkiae, 185, 186
longipes, 186, 189
nitidum, 189
parasiticum, 187
rude, 189
squamosum, 186, 189
subtrigonum, 186
Leptonacea, 419, 423, 424
Leptosynapta, 188
inhaerens, 188
ooplax, 188
Leptoxis, 9, 58
Leptychaster, 115
lepomis, Plagioporus, 10
lewisii, Pleurocera, 56, 58
libertina, Semisulcospira, 3
Libratula, 184
plana, 184
lignarius, Scaphander, 359, 361
Liguus, 424
Limanda, 198
ferruginea, 198
Limapontia, 342, 353-357, 365, 370
capitata, 365
Limapontiidae, 365
limosa, Amnicola,
linda, Haminoea,
lineolata, Chromodoris,
Lissodoris, 247
Lithasia, 8, 9, 38, 58, 73
venusta, 58
Lithasiopsis, 9
Lithoglyphus, 105, 107
Lithophaga, 183
Litigiella, 185
glabra, 185
liturata, Discodoris, 275
Littorina, 35, 337, 400
littorea, 400
livescens barronensis, Goniobasis, 55
livescens correcta, Goniobasis, 9, 36,
38, 53, 55, 56
livescens, Goniobasis, 1-80
livescens michiganensis, Goniobasis,
53
42, 43
235, 236, 241-244
264, 272
livida, Elysia, 270
Lobiger, 356
Loligo, 287, 288, 303, 304
opalescens, 288, 303, 304
vulgaris, 287, 288, 303, 304
lonca, Catriona, 263, 264, 274, 275, 279,
280
236, 244, 264,
267
longicauda, Stylocheilus,
longicirrha, Ennoia, 283
longicornis, Myja, 280
longinqua, Amnicola, 104, 108
longinqua, Paludestrina, 104
longinqua, Fontelicella, 108
longipes, Ceratobornia, 186
longipes, Lepton, 186, 189
longissima, Eunereis, 186
lora, Discodoris, 263, 268, 269, 273-
275
452
Loxosoma, 185, 186
Lucinacea, 419-425
Lucinidae, 422, 424
ludwigi, Entocolax, 117, 143
lugubris, Pleurobranchus, 264, 271
lunata, Ephippodonta, 184, 189
lunulata, Harmothoé, 189
luteola, Lampsilis, 10
luteopunctata, Doridopsis nigra, 250
lutescens, Discodoris, 276
luteus, Phanerophthalmus, 263, 264
53, 311, 385, 420, 428
stagnalis, 53, 311, 420
lyrifera, Brissopsis, 187
Lysiosquilla, 183, 189
maculata, 189
scabricauda, 189
lysiosquillina, Phlyctaenachlamys,
lyttonensis, Io fluvialis, 35
macdougalli, Ephippodonta,
macrostoma, Proterometra,
Mactromyidae, 422, 424
maculata, Gymnodoris,
maculata, Lysiosquilla,
maculata, Onchidella, 256
maenas, Carcinides, 189
magdalenensis, Ischnochiton,
magnifica, Doris, 249
maillardi, Dolabrifera,
major, Entovalva, 188
major, Callianassa, 189
major, Upogebia, 189
maoria, Divariscintilla, 189
marenzelleri, Hypselodoris,
marginata, Elysia, 264, 270
marginata, Lehmannia, 311
marginatus, Hexabranchus,
Marikellia, 184, 186
vincentensis, 184
mavrilandia, Quercus,
Mastogloia, 69
smithü, 69
smithii cryptocephala,
maua, Catriona, 279
maxillosus, Polydontes, 186
meckelii, Pleurobranchaea, 348
mediterranea, Caliphylla, 356
mediterraneum, Pneumoderma,
Lymnaea,
189
184, 189
70, 71
250
189
186
244
273
264, 271
45
69
365
Megadenus, 116, 129, 134, 138, 143, 151,
172-175
arrhynchus, 116, 129, 134, 151, 172-
175
MALACOLOGIA
holothuricola,
voeltzkowi, 143, 173
cysticola, 151
melaena, Dendrodoris, 250
Melanella, 138, 151, 175
equestris, 151
polita, 151
Melanellidae,
Melania, 8,9
virginica, 35
Melanogrammus,
aeglefinis, 198
Melanoides, 1
tuberculatus, 1
Melanopsis, 22
dufourei, 22
Melosira, 68
ambigua, 68
varians, 68
meridionalis, Spatangus,
Mertensiothuria, 188
fuscocineria, 188
Mesodon, 311
appressa, 311
Mesogastropoda, 229, 231, 335, 344, 345
Miamirinae, 264, 273
michelini, Heteropsammia, 185
michiganensis, Goniobasis livescens,
micra, Amnicola, 104, 108
micra, Fontelicella, 108
Micrasterias, 67
radiata, 67
Microamnicola, 103, 109
micrococcus, Amnicola,
micrococcus, Fontelicella,
Microhedylidae, 357
Micromya, 42, 43
iris, 42, 43
Microspora,
floccosa,
Miesea,
evelinae,
mietta, Herviella,
miliaris, Lasaea,
mimetica, Bosellia, 353
minima, Navicula, 69
minor, Navicula tuscula,
minuta, Diaphana, 364
minutissima cryptocephala, Achnanthes,
68
134, 143, 174
111-181
198
187
53
103, 109
109
67
67
279, 351, 372
279, 351
235, 252, 253
186
69
68
117
minutissima, Achnanthes,
mirabilis, Entoconcha,
INDEX, VOL. II
mirabilis, Entovalva, 188
missouriense, Ribes, 45
Mitra, 185
modesta, Alderia, 354
Mollusca, 184, 186
Molpadicola, 135, 145, 172-175
orientalis, 135, 145, 172
Monoplacophora, 419
Monotocardia, 171
Montacuta, 184-187
christenseni, 187
donacina, 188
echinocardiophila, 187
ferruginosa, 187
glabra, 185
percompressa, 188
perezi, 185
phascolionis, 185, 186
semiradiata, 187
substriata, 187
morhua, Gadus, 198
Moridilla, 282
Morula, 211-233
granulata, 211-233
nodus, 212
Moroteuthis, 287-307
ingens, 287-307
robsoni, 289, 299
mucosum, Thalassema, 185
Mucronalia, 129, 138, 173, 175
eburnea, 129
variabilis, 173, 175
Muessa, 263, 264, 280-283
evelinae, 263, 264, 280-283
Mudalia, 8, 9, 35, 72
dissimilis, 35
muloc, Antiopella, 351
multicarinata, Goniobasis, 10
multiformis, Brachidontes, 186
multiformis, Hormomya, 186
murakamii, Ephippodonta, 184
Murex, 185, 228, 229
erinaceus, 231
fulvescens arenarius, 229
pomum, 229
Muricacea, 211, 230
muricata, Onchidoris, 365
musetta, Haminoea, 235, 236, 239, 241
mutabilis, Goniobasis, 36
Mya, 399-418
avenaria, 399-418
truncata, 399-418
truncata ovata, 399-418
pseudoarenaria, 399-418
truncata typica, 399-418
truncata uddevallensis, 399-418
myaciformis, Pseudopythina, 189
Myja, 280
longicornis, 280
Mylitta, 184, 189
deshayesiana, 189
gemmata, 189
tasmanica, 189
Myriophyllum, 45
tenellum, 45
Mysella, 183-189
bidentata, 183-189
Mytilus, 186, 189
californianus, 186
edulis, 189
nana, Akera, 186
Nassarius, 185
trivattatus, 185
Natica, 203
clausa, 203
Nasturtium, 45
officinale, 45
natans, Potamogeton, 45
Natricola, 103, 108, 109
Nautilus, 379
Navicula, 67, 69
cryptocephala, 69
cryptocephala veneta, 69
exigua, 69
gractlis, 67
lacustris, 69
minima, 69
oblonga, 69
pupulla, 69
vadiosa, 67, 69
radiosa tenella, 69
rhynococephala, 67, 69
rostella, 69
tuscula, 69
tuscula minor, 69
viridula, 69
navicula, Haminoea, 364
naviculiformis, Cymbella, 68
neapolitana, Spurilla, 351
Nembrotha, 250, 264, 277
nigerrima, 264, 277
Neopilina, 419, 420
Nereis, 186
neritea, Cyclope, 221, 229
neuvillei, Cyrtodaria, 202, 203
nicaraguana, Dolabrifera, 244
453
454
nigerrima, Nembrotha, 264, 277
nigra, Cyerce, 264, 269
nigra, Dendrodoris, 236, 250, 264, 277
nigva, Doris, 250
nigra luteopunctata, Doridopsis, 250
nigricans, Onchidella, 256
nigricans, Occidentella, 256
nigrocincta, Aplysia parvula, 266
nigrocincta, Pruvotaplysia parvula, 266
nigropunctata, Haminoea, 240
nigrostriata, Hypselodoris, 273
Nipponomontacuta, 184
actinariophila, 184
Nitella, 45
flexilis, 45
nitidum, Lepton,
Nitocris, 9, 36
carinata, 36
Nitzschia, 69
acicularis, 69
hantzschiana, 69
sinuata, 69
nobilis, Anisodoris,
nobilis, Phyllidia,
nobilis, Phyllidiella,
nodus, Morula, 212
nonatoi, Costasiella, 267
Nonsuctoria, 236, 264, 277
normani, Cymbella, 68
nosophora, Oncomelania,
Notarchus, 364
Notarchinae, 236, 264, 267
Notaspidea, 264, 271, 345, 346, 371, 372
noto, Ercolania, 269
noto, Stiliger, 269
noumeae, Globiferina, 283
Noumeaella, 263, 264, 274, 275, 280-
282
189
338
264, 278
264, 278
82, 97, 98
282
263, 264, 274, 275, 280-282
229, 231, 386
229, 231
421
264, 271, 345, 365, 372
185
curiosa,
rehderi,
Nucella,
lapillus,
Nuculanidae,
Nudibranchia,
nudus, Sipunculus,
Nuphar, 45
variegatum, 45
Numphaea, 45
odorata, 45
oblonga, Navicula, 69
oblonga, Serridens, 186
obscura, Glossodoris, 273
MALACOLOGIA
obscura, Occidentella, 254
obscura, Onchidella, 254
occidentalis, Blepharipoda,
occidentalis, Cotylogaster,
Occidentella, 254, 256
nigricans, 256
obscura, 254
reticulata, 256
ocellata, Bouvieria, 348
ocellatus, Plakobranchus,
ocellifera, Costasiella,
odorata, Nymphaea, 45
Odostomia, 175, 185
perezi, 185
Oegopsida, 287
officinale, Nasturtium, 45
ohshimai, Entovalva, 188
ohshimai, Fronsella, 185
ohshimai, Peregrinamor,
Ommastrephes, 288
sloanei, 288
Onchidella, 235, 253, 255, 256, 367
celtica, 254
evelinae, 235, 253, 255, 256
flavescens, 256
maculata, 256
nigricans, 256
obscura, 254
palelloides, 254, 256
reticulata, 256
Onchidellidae, 254
Onchidiacea, 236, 254, 263, 264
Onchidiidae, 236, 263, 264, 327, 366,
367
189
69, 70, 72
264, 270
267
189
Onchidorididae,
Onchidoris, 365
muricata, 365
Oncomelania, 29, 40, 60, 81-102
formosana, 81-102
hupensis, 82, 97, 98
nosophora, 82, 97, 98
quadrasi, 60, 99, 100
Onychoteuthidae, 287, 289
ooplax, Synapta, 188
365
ooplax, Leptosynapta, 188
Ophiocnida, 188
brachiata, 188
Ophiuroidea, 88
Opisthobranchia, 327-378
oratoria, Squilla, 189
135, 145, 172
269
orientalis, Molpadicola,
orientalis, Phyllobranchillus,
INDEX, VOL. Ш
ornata, Elysia, 270
Oscaniella, 271
purpurea, 271
Ostrea, 226, 400
ovalis, Haminoea, 243
ovalis, Succinea, 311, 322
Oxyloma, 310
Oxynoacea, 364, 366
Oxynoe, 356, 364
Oxynoidae, 364, 370
Oxytrema, 8, 71
Pachychilus, 9
Pachymania, 22
pacifica, Petalifera petalifera, 264, 267
Padina, 266, 270
Paedophoropodidae, 112, 115, 126, 138,
146, 159, 166-175
Paedophoropus, 135, 138, 145, 151, 168,
170-175
dicoelobius, 138, 151, 168, 172
Paliolla, 250
pallida, Discodoris, 275, 276
pallida, Embletonia, 351
palma, Discodoris, 276
Paludestrina, 104, 108
cedrosensis, 104, 108
longinqua, 104
stearnsiana, 104
paludosa, Pomacea, 419-431
palustris, Quercus, 45
pancerii, Ercolania, 267
pancerii, Stiliger, 267
papillosa, Aeolidia, 345, 351
papyrifera, Betula, 45
Parabornia, 184, 189
squillina, 189
Paragonimus, 3
westermani, 3
parallela, Rhopolodia, 69
parasiticum, Lepton, 187
Parastilifer, 129, 134, 138, 173, 175
sibogae, 134
Parenteroxenos, 117, 133, 170, 175
parma, Echinarachnius, 200, 201
Partulida, 365
spiralis, 365
parvula, Aplysia, 263, 266
parvula nigrocincta, Aplysia, 266
parvula nigrocincta, Pruvotaplysia,
parvula, Pruvotaplysia, 263, 266
patelloides, Onchidella, 254, 256
266
455
188
188
Patinapta,
crosslandi,
laevis, 188
pediculus, Cocconeis, 68
pedroana, Rochefortia, 189
pellucida, Amphipleura, 69
pellucida, Polybranchia, 269
pellucidum, Phascolosoma, 185
Pelseneeria, 143,151, 163, 169, 172, 175
stylifera, 143, 163, 169
Pelseneeriidae, 112, 172, 175
percompressa, Montacuta, 188
Peregrinamor, 184, 189
ohshimai, 189
perezi, Auristomia,
perezi, Montacuta,
perezi, Odostomia,
Peronia, 263, 264
peronii, 263, 264
peronii, Peronia, 263, 264
peronii, Pleurobranchus, 264, 271
perrieri, Devonia, 188
perrieri, Entovalva, 188
petalifera pacifica, Petalifera,
Petalifeva, 264, 267, 364
petalifera pacifica, 264, 267
pfeifferi, Biomphalaria, 379-398
Phanerozonia, 115
pilsbryana, Amnicola,
pilsbryana, Fontelicella,
pilsbryi, Amnicola, 108
Pinnularia, 67, 69
lata, 69
viridis, 67
Pinus, 45
vesinosa, 45
Phanerobranchia,
Phanerophthalmidae,
Phanerophthalmus,
luteus, 263, 264
Phascolion, 185, 186
strombi, 185, 186
phascolionis, Montacuta,
Phascolosoma, 185
elongatum, 185
pellucidum, 185
Philinacea, 236, 263, 265
Philine, 337, 341, 359-364
alba, 359, 361
aperta, 359, 361, 362
scabra, 364
185
185
185
264, 267
104, 108
108
236, 264, 277
263, 265
239, 263, 264, 370
185, 186
456 | MALACOLOGIA
Philinidae, 340, 341, 357, 360-371
Philinoglossa, 370
Philinoglossidae, 327, 358, 366, 370,
371
philippi, Tripylaster, 187
Phlyctaenachlamys, 184, 189
lysiosquillina, 189
Phyllidia, 264, 277, 278
nobilis, 264, 278
pustulosa, 264, 278
varicosa, 264, 277
Phyllidiella, 264, 278
nobilis, 264, 278
pustulosa, 264, 278
Phyllidiidae, 264, 277
Phyllobranchillidae, 264, 269
Phyllobranchillus, 264, 269
orientalis, 269
prasinus, 269
Phyllodesmium, 264, 280, 283
hyalinum, 264, 280, 283
Physa, 42, 43, 311, 429
acuta, 311,
gyrina, 42, 43
integra, 42, 43, 429
placentula, Cocconeis, 68
plactorhychus, Axius, 189
Plagioporus, 69, 70
lepomis, 10
sinitsini, 69, 70
sinitsini huroni, 10
Plakobranchidae, 264, 270
Plakobranchus, 264, 270
ocellatus, 264, 270
plana, Libratula, 184
Planorbidae, 379
platessoides, Hippoglossoides, 198
Platydoridinae, 264, 277
Platydoris, 264, 277
cruenta, 264
flammulata, 264, 277
scabra, 264, 277
Pleurobranchacea,
Pleurobranchaea,
hamva, 348
meckelii, 348
Pleurobranchidae, 264, 271, 366, 372
Pleurobranchus, 264, 271
lugubris, 264, 271
peronii, 264, 271
Pleurocera, 1-80
acuta, 1-80
264, 271
347, 348, 364
acutum tractum, 10
canaliculata, 9, 36, 58, 63
canaliculatum undulatum,
curtum, 36
lewisii, 56, 58
subulare, 10, 35
subulareforme, 36
unciale, 36
unciale curtatum, 36
verrucosa, 8,9
Pleuroceridae, 106
Pneumoderma, 362, 365
mediterraneum, 365
Pneumodermatidae, 365
polaris, Leptasterias, 115
polita, Melanella, 151
Polybranchia, 269
pellucida, 269
Polydontes, 186
maxillosus, 186
Polygyra, 311
appressa, 311
Polygyridae, 311
Pomacea, 419-431
paludosa, 419-431
pomatia, Helix, 311, 420
Pomatiopsinae, 104
9, 18-40
Pomatiopsis, 29, 40, 82, 99, 103, 108,
109
cincinnatiensis, 29, 82, 99
intermedia, 104, 108
robusta, 103, 109
Pomatogeton, 45
natans, 45
praelongus, 45
vichardsonii, 45
Pomoxis, 10
sparoides, 70
pomum, Murex, 229
Populus, 45
heterophylla, 45
Porifera, 184
Porostomata, 236, 264, 277
Portlandia, 205, 400
aestuariorum, 205
arctica, 400
Potadoma, 22
Potidoma, 184-186
clarkiae, 185
subtrigona, 186
praelongus, Pomatogeton, 45
prasinus, Phyllobranchillus, 269
INDEX, VOL. II
245
103571225113, 171, 231,
331, 343, 345
prostrata, Cymbella, 68
Protankyra, 187
bidentata, 188
similis, 188
Proterometra,
macrostoma, ‘10, 71
sagittaria, “0, 71
Protococcus, 67
viridis, 67
Pruvotaplysia, 263, 266
parvula, 263, 266
parvula nigrocincta, 266
proxima, Goniobasis, 36
Pseudopythina, 184, 186, 189
compressa, 189
myaciformis, 189
rugifera, 186, 189
subsinuata, 189
Pseudosacculidae,
Pseudosacculus,
Pseudovermis,
Pteraeolidia,
semperi, 264, 280
Pterotrachea, 420
pugettensis, Upogebia, 189
pulchella, Goniobasis, 70
pulchella, Vallonia, 311
pulchellum, Dictyosphaerium, 67
Pulmonata, 311, 343, 366, 367
pulmonica, Aplysia, 263, 266
pulmonica, Varria, 263, 266
punctata, Aplysia, 364
preciosa, Doris,
Prosobranchia,
70, 71
171
114
351, 372
264, 280
punctocaelatus, Acteon, 336-338
pupulla, Navicula, 69
purpurea, Oscaniella, 271
purpureus, Spatangus, 187
pustulosa, Phyllidia, 264, 278
pustulosa, Phyllidiella, 264, 278
putris, Succinea, 311
Pyramidellidae, 171, 172, 175, 343, 345,
351, 352, 357, 365, 366
Pythinella, 185
cuneata, 185
quadrasi, Oncomelania, 99, 100
Quercus, 45
alba, 45
coccinea, 45
marilandia, 45
palustris, 45
457
radiata, Micrasterias, 67
vadicans, Rhus, 45
vradiosa, Navicula, 67, 69
radiosa tenella, Navicula, 69
vansoni, Hypselodoris, 273
тата, Elysia, 263, 264, 268-271
rehderi, Noumeaella, 263, 264, 275, 280-
282
vesinosa, Pinus, 45
veticulatus, Lebistes, 14
reticulata, Occidentella,
reticulata, Onchidella,
retroversa, Spiratella,
Retusa, 263, 264
Retusidae, 263, 265, 327, 357, 358, 366,
370, 371
256
256
365
Rhizorus,
Rhodope, 346
Rhopalodia, 67, 68
gibba, 67, 68
parallela, 69
Rhus, 45
copallina, 45
vadicans, 45
vernix, 45
rhynococephala, Navicula,
Ribes, 45
missouriense, 45
richardsonii, Pomatogeton, 45
vicina, Drupa, 211-233
rimsky-korsakovi, Entocolax,
360, 371
67, 69
143, 170,
174
346
346
Ringicula,
Ringiculidae,
Risbecia, 247
Rizzolia, 253
robusta, Fontelicella,
robusta, Pomatiopsis,
Rochefortia, 189
pedroana, 189
Rochelfortia, 184, 185
cuneata, 185
vostella, Navicula, 69
rotundata, Catinella, 309, 310, 313, 321
109
103, 109
rotundata, Haminoea, 243
rubra, Dendrodoris, 250
rubra, Kellia, 185, 186
rubra, Lasaea, 187
rubrum, Acer, 45
rude, Lepton, 189
rufomarginata, Casella, 264, 273
vugifeva, Pseudopythina, 186, 189
458 MALACOLOGIA
rugosus, Strophitus, 42, 43 siliqua, Cyrtodaria, 197-210
rugulosus, Anthenoides, 116 siliquoidea, Lampsilis, 42, 43
Runcina, 331, 334, 358, 360, 370, 371 simillima, Haminoea, 241
runcinata, Chromodoris, 248 sinensis, Clonorchis, 3
runcinata, Hypselodoris, 273 sinitsini huroni, Plagioporus, 69, 70
Runcinella, 360 sinitsini, Plagioporus, 69, 70, 71
Runcinidae, 327, 358, 360, 366, 370, 371 sinuata, Nitzschia, 69
rupestris, Ambloplites, “0 Siphonaria, 236, 256, 257, 367
rüppelli, Fryeria, 264, 279 cochleariformis, 257
Sacculosiphonaria, 236, 256, 257 guamensis, 236, 255, 256, 257
cochleariformis, 257 Siphonariacea, 236
guamensis, 236, 256, 257 Siphonariidae, 236
Sacoglossa, 264, 267, 327, 337, 352- Sipuculus, 185
354, 364, 369, 370 nudus, 185
Sagittaria, 45 Sipunculoidea, 184, 185
latifolia, 45 Smaragdinella, 236-238
sagittavia, Cercaria, 1 calyculata, 236-238
sagittavia, Proterometra, ‘0, 71 glauca, 236, 238
Salvelinus, 171 viridis, 236, 238
fontinalis, 71 | Smaragdinellidae, 236
scabra, Philine, 364 smaragdinus, Lathophthalmus, 236, 238
scabra, Platydoris, 264, 277 smithii cryptocephala, Mastogloia, 69
scabricauda, Lysiosquilla, 189 smithii, Mastogloia, 69
scalaris, Lasaea, 186 smithi, Hermaeina, 336, 353, 365
Scaphander, 337,359, 360, 361, 369, 371 Soleolifera, 236, 263, 264
lignarius, 359, 361 solitaria, Haminoea, 364
Scaphandridae, 357-371 sparoides, Pomoxis, 10
scapula, Dolabella, 266 Spatangus, 187
schiemenzi, Entocolax, 117 mevidionalis, 187
Schistosoma, 81 purpureus, 187
japonicum, 81 Sphaerocystis, 67
schroeteri, Sphaerocystis, 67 schroeteri, 67
schwanwitschi, Entocolax, 151, 159, 160, sphaerophora, Anomoeoneis, 67.
163, 170 Spinulosa, 115
Scintillona, 184, 188 spiralis, Partulida, 365
zelandica, 188 Spiratella, 362, 363, 365
Scioberetia, 184, 187 retroversa, 365
australis, 187 Spiratellidae, 365
Scirpus, 45 Sphaerumbonella, 184
americanus, 45 brunelli, 184
semiradiata, Montacuta, 187 splendida, Aglaja, 263, 264
Semisulcospira, 3 Spondylus, 186
libertina, 3 Spurilla, 351
semperi, Entovalva, 188 neapolitana, 351
semperi, Hypselodoris, 273 Spyrogyra, 14, 45
semperi, Pteraeolidia, 264, 280 stagnalis, Lymnaea, 53, 311, 420
Sepiidae, 288 Stagnicola, 311
Serridens, 184, 186 emarginata, 311
oblonga, 186 Staurastrum, 67
shimekii, Ferrissia, 60 furcigerum, 67
sibogae, Parastilifer, 134 Stauroneis, 67, 69
sibogae, Stilifer, 129 anceps, 67, 69
stearnsiana, Fontelicella,
stearnsiana, Paludestrina, 104
stellata, Upogebia, 189
Stenoglossa, 211, 230, 231
Stiliferidae, 112-181
Stilifer, 116, 129, 135, 138, 151, 163,
172, 173, 175
celebensis, 135, 138, 151, 172
sibogae, 129
stylifer, 163
Stiligeridae, 264, 267, 365
Stiliger, 263, 264, 267-269, 356
akkeshiensis, 269
illus, 263, 264, 267-269,
noto, 269
pancerii, 267
trinchesei, 269
stolonifera, Cornus, 45
Stomatopoda, 189
Strephobasis, 9
striata, Trevelyana, 250
strombi, Phascolion, 185, 186
Strombus, 35
Strophitus, 42, 43
rugosus, 42, 43
stylifera, Pelseneeria,
stylifer, Stilifer, 163
Stylocheilus, 236, 244, 264, 267
‚ longicauda, 236, 244, 264, 267
Stylommatophora, 309, 311
Stylophora, 278
subglobosa, Anculosa, 36
subsalina, Fragilaria construens,
subsinuata, Pseudopythina, 189
substriata, Monacuta, 187
subtile, Gomphonema, 68
subtrigona, Potidoma, 186
subulaeforme, Pleurocera, 36
subulare, Pleurocera, 10, 35
subtrigonum, Lepton, 186
subviridis, Lasaea, 186
Succinea, 310
avara, 310
campestris vagans, 310
hivasei, 311, 321
horticola, 311, 321
kwansae, 311, 321
ovalis, 311, 321, 322
putris, 311, 321
vagans, 310
Succineidae, 309, 311, 321
suecica, Hedylopsis, 365
INDEX, VOL. II
107, 108
143, 163, 169
68
susa, Catriona, 280
squamosum, Lepton,
Squilla, 189
oratoria, 189
squillina, Pavabornia, 189
Synapta, 188
186, 189
ooplax, 188
Synapticola, 184, 188
Synedra, 68
ulna, 68
vaucheriae, 68
Tabellaria, 67, 68
fenestra, 67, 68
Taenioglossa, 151, 171, 174
Tambja, 250
Tancrediidae, 422, 424
Tapes, 400
Tarebia, 3
tasmanica, Mylitta, 189
tenella, Navicula radiosa, 69
tenellum, Myriophyllum, 45
tenuilinearis, Hypselodoris, 273
teresiae, Turricula, 186
Tetronychoteuthis, 289
texana, Cateinella, 309, 310, 321
Thaira, 3
granifera, 3
Thalassema, 185
mucosum, 185
thalassemicola, Achasmea, 185
Thecosomata, 362-368
thomasi, Ulmus, 45
Thyasiridae, 422, 424
Thyonicola, 117
Thyreopsis, 184
coralliophila, 184
thysanopoda, Elysia,
Todarodes, 288
sagittatus, 288
tomentosa, Carya, 45
tornatilis, Acteon, 337, 338
Tornatina, 358
torquata, Clymenella, 186
tractum, Pleurocera acutum, 10
transcaspica, Cyrtodaria,
Trevelyana, 249, 250
bicolor, 249
striata, 250
Trichomya, 186
hirsuta, 186
Tridachia, 356
crispata, 356
264, 270
202, 203
459
460 MALACOLOGIA
Triopha, 333, 345
carpenteri, 333, 345
trinchesei, Ercolania, 269
trinchesei, Stiliger, 269
Tripylaster, 187
philippi, 187
Tripylus, 187
triquetra, Dysnomia, 42
Tritonia, 345, 350, 351, 365
hombergi, 345, 365
Tritoniidae, 365
Trivia, 229, 231
trivittatus, Nassarius, 185
trivolvis, Helisoma, 11, 42, 43
Trochodota, 188
dendyi, 188
trochodotae, Entocolax, 117, 151, 159
Trochus, 381
truckeensis, Fontelicella, 108
truckeensis, Hydrobia, 104
Trypanostoma, 9
tuburculata, Archidoris, 365
tuberculatus, Melanoides, 3
tumidus, Unio, 410
Turbo, 226
Turbonilla, 175
turgida, Epithemia, 67
turnbullae, Ephippodonta, 184, 189
Turricula, 186
teresiae, 186
Turritella, 185
communis, 185
tuscula minor, Navicula, 69
tuscula, Navicula, 69
Typha, 45
latifolia, 45
Tyrinna, 276
Ulmus, 45
thomasi, 45
ulna, Synedra, 68
Ulva, 212
fasciata, 212
Umbraculidae, 366, 372
Unbraculum, 346, 371
unciale curtatum, Pleurocera, 36
unciale, Pleurocera, 36
undulatum, Pleurocera canaliculatum,
9, 18, 21-40
Ungulinidae, 422
Unicardiidae, 422
Unio, 410
tumidus, 410
Unionidae, 183
Upogebia, 186, 189
affinis, 189
deltaura, 189
major, 189
pugettensis, 189
stellata, 189
Urosalpinx, 226
cinerea, 226
urquisa, Catriona, 263, 264, 274, 275,
279, 280
uva, Doto, 351
vagans, Catinella, 310
vagans, Succinea, 310
vagina, Cyrtodaria, 203
vagum, Batrachospermum, 45, 68
Vallisneria, 45
americana, 45
Vallonia, 311
pulchella, 311
variabilis, Mucronalia, 173, 175
varians, Melosiva, 68
varicosa, Phyllidia, 264, 277
variegata, Dolabrifera, 244
variegatus, Chlorella, 67
variegatum, Nuphar, 45
Varria, 263, 265, 266
dactylomela, 263, 265
pulmonica, 263, 266
Vasconiella, 184, 189
vaucheriae, Synedra, 68
veneta, Navicula cryptocephala, 69
ventricosa, Cymbella, 68 .
venusta, Chromodoris, 264, 272
venusta, Lithasia, 58
vermeta, Catinella, 309-325
Vermetus, 186
corallinaceus, 186
vernix, Rhus, 45
verrucosa, Angitrema, 9
verrucosa, Pleurocera, 8
vibrio, Gomphonema, 67
vincentensis, Marikellia, 184
virginicum, Buccinun, 8
virginicum, Goniobasis, 8, 35, 36, 51,
,
vivgula, Creseis, 333, 365
Virgulate, 10
xiphidiocercariae, 70
viridis, Elysia, 356
viridula, Navicula, 69
viridis, Pinnularia, 67
eg =
INDEX, VOL. Ш
viridis, Protococcus, 67 westermani, Paragonimus, 3
viridis, Smaragdinella, 236, 238 xiphidiocercariae, Virgulate, 70
Vites, 45 yatsui, Herviella, 251, 253, 283
aestivalis, 45 ylva, Discodoris, 263, 274-276
vitrea, Haminoea, 243 Yoldia, 400
Vitrohaminoea, 240 arctica, 400
voeltzkowi, Megadenus, 143, 173 Yoldiella, 203
Volutacea, 230 frigida, 203
voniheringi, Discodoris, 349 zebra, Epithemia, 68
vulgare, Golfingia, 184 zelandica, Scintillona, 188
vulgaris, Chara, 45 Zizyphinus, 185
vulgatum, Cerithium, 22 conuloides, 185
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MALACOLOGIA 463
ABCTPAKT
СИМБИОТИЧЕСКИЕ ДВУСТВОРЧАТЫЕ НАДСЕМЕЙСТВА ERYCINACEA
Кеннет Босс
Эта работа суммирует случаи симбиотического поведения между пред-
ставителями пластинчатожаберных моллюсков надсемейства Erycinacea.
Отдельные случаи комменсализма, мутуализма, даже эктопаразитизма, и, Ka-
жется, эндопаразитизма представлены со всеми данными. Моллюски тут рас-
сматриваются с точки зрения их отношений к хозяевам и в конце приложены
некоторые замечания относительно причин таких симбиотических сожительств.
АБСТРАКТ
"КОЛЬЦА РОСТА" НА КЛЮВЕ КАЛЬМАРА MOROTEUTHIS INGENS)
(OEGOSIDA: ONYCHOTEUTHIDAE)
Мальколвм P. Кларкз
Настоящая работа, с описанием циклов линий наростания на нижней
мандибуле у Moroteuthis ingens, предлагается с целью обратить внима-
ние на возможную связь циклами развития и временем роста кальмара. Это
исследование основано на большом отборе клювов, добытых из желудков Ka-
шелотов, пойманных у Дурбана. Тут описаны характерные особенности, KOTO-
рые были использованы для определения (см. фиг. 1). В средней части бо-
ковой поверхности стенок этих клювов заметны 4 особенности (фиг. 2): бороз-
ды расходятся радиусами от кончика клюва до свободного края и параллельно
ему, мелкие порожки или микрокольца и волнистые линии различной прозрач-
ности. Микрокольца являются конечным пределом во время роста боковых
стенок. Циклы ширины микроколец между кончиком и свободным краем ясно за-
метны. Варианты формы циклов в 50 клювах описаны и покано, что первые 3-
4 цикла обыкновенно следуют по определенному рисунку, в то время как после-
дующие значительно рознятся (фиг. 3). В продолжение жизни животного кон-
чик клюва претерпевает очень мало изнашивания (ростральная длина колеб-
лется между 0.7 и 2.0 см). Частота гистограми и среднее количество ми-
кроколец каждого цикла указывают, что эти циклы не являются произвольными
колебаниями только одной секреции, если бы даже эти колебания были диаго-
нальными по отношению к последующим циклам и более узкими, чем предыдущие
циклы. Рост клюва может быть выражен как увлечение длины стенок, т.е.
расстояние между кончиком клюва и передним и внутренним углом боковой
стенки (фиг. 2). Так как процесс роста длины стенки регистрируется рас-
стоянием микроколец от конца клюва, то рост можно высчитать в обратном
порядке. Увеличение размеров клюва с увеличением числа циклов было про-
эктировано, также как расчет кривой в обратном порядке, зависит не от от-
бора автора, а от выбора пищи кашелотов (фиг. 8). Обратный расчет длины
стенки среди клювов постарше (с большим количеством циклов) выражен был
более низкими цифрами, чем среди более молодых, вероятно, потому что мед-
464 MALACOLOGIA
леннее растущие особи кальмаров живут дольше. Было проэктировано COOT-
ношение длины стенки с размерами кальмаров (фиг. 10, 11). Время, Heo6xo-.
димое для образования одного цикла, установлено не было, HO на основании |
прежних исследований других головоногих можно предложить, ‘что этот период.
может быть от 6 U до 12 месяцев.
АБСТРАКТ
МОРФОЛОГИЯ И ИСТОРИЯ ЖИЗНИ PLEUROCERA ACUTA И GONIOBASIS LIVESCENS
(GASTROPODA: CERITHIACEA: PLEUROCERIDAE)
Бонифаций Капили Дазо
Сравнительно мало известно о семействе пресноводных крышечных ули-
ток Pleuroceridae распространенных в Северной Америке, охватывающих
или же родственных чернушкам, которые важны для паразтологии Дальнего
Востока. Систематика их основана главным образом на характере раковины
и нуждается в пересмотре. Произведены исследования 2-х видов, отнесен-
ных к 2-м различным родам: Pleurocera acuta Rafinesque и Goniobasis
livescens (Menke), взятые из 4-х участков в районе Анн Ap6op, штата
Мичиган и из других мест в штатах Мичиган и Охайо, в США.
Раковины и крышечки этих 2-х видов различны, но их анатомия и образ
жизни настолько значительно близки, что их принадлежность к 2-м отдель-
ным родам становится сомнительной.
Различия в строении их раковин, хотя и вполне заметны, но не яв-
ляются постоянными и почти незаметны в некоторых промежуточных особях.
Pleurocera acuta приблизительно вдвое больше С. livescens.
Хотя общая форма и пигментация тела очень сходны, но P. acuta OTIANMUaAET-
ся более продолговатыми головой и хоботом и более длинными и более кону-
сообразными щупальцами. У Р. асша нога меньше и более удлиненной
формы, что, возможно, является приспособлением к жизни на дне и к рытью,
в TO время как у С. livescens нога больше и круглее в сравнении с
передней частью тела, что можно связать с привычным ползанием. Мантия
и органы чувств, общая нервная система, морфология.дыхательной, выдели-
тельной, кровеносной и мускульной систем у обоих видов очень сходны; раз-
нятся они только размерами. У подсемейства Pleurocerinae y самцов от-
сутствует пенис. У самок глубокое углубление в шее между правым щупаль-
цем и подошвой ноги, а также мелкая канавка, ведущая к этому углублению,
служат как органы размножения. В остальном общая схема органов размно-
жения совпадает с таковыми у других переднежаберных моллюсков. Эти мол-
люски раздельно - полые. В обоих видах органы размножения у каждого пола
почти идентичны и находятся в том же положении. Сперма у них 2х типов:
типичная эупиренная и ненормальная апиренная Формы. Эупренная сперма пе-
редается самке в сперматофорах. к
Северо-американские переднежаберные нуждаюся в чистой воде...
За исключением рода Goniobasis они предпочитают сравнительно более
просторные места. Обыкновенно они в песчанных или илистых частях про-
точной воды под прикрытием. С. livescens живет почти везде в чисто и
проточной пресной воде (будь то ручей, быстрая река или озеро), этот
вид обыкновенно наблюдается ползающим по камням.
MALACOLOGIA 465
Оба наблюдения, как в природе, так и в лаборатории, указывают, что
спаривание происходит осенью. Когда температура падает ‘ниже 50 граду-
сов, улитки начинают зимнюю спячку. Весной они возвращаются к актив-
ности и кладут яйца. Яйца P. acuta покрытые песком кладутся в массах
различного размера и формы, количество яиц в каждой массе колеблется
между 1 и 19. С. livescens кладет яйца по одиночке или по 2 - Зв ряд
с промежутком в несколько CM., они обыкновенно покрываются тонким слоем
ила. Р. асша кладет больше яиц (15 яиц на самку в день), чем С.
livescens (около 4-х), но у нее этот период короче (от апреля до июня),
тогда как С. livescens кладет яйца от апреля до половины августа. У
обоих видов эмбриональное развитие продолжается 2 недели.
Во время первого года жизни происходит наиболее заметный рост (от
Crna HO LO MM y AP. acuta; oT 0.3 до 0.8 мм УС. livescens). Когда выросшие
в лаборатории улитки достигают половой зрелости, в 2 года они были в
16.7 ив 7.0 мм в диаметре, после чего рост их был незначительным.
Продолжительность их жизни в нормальных условиях - 3, может быть, 4 года.
У Р. acuta количество самцов к количеству самок равно 1:2, а у С.
livescens -1:5. Как и другие виды переднежаберных, самцы и самки
обоих видов питаются красными, зелеными, десмидиевыми и диатомными водо-
рослями. В печени, пищеводе и других органах зачастую паразитируют ли-
чинки сосальщиков, главным образом из семейств Azygiidae, Allocreadiidae,
Aspidogastridae.
ABCTPAKT
, КОНХОМЕТРИЯ ПРЕСНОВОДНОЙ УЛИТКИ BIOMPHALARIA PFEIFFERI
(BASOMMATOPHORA: PLANORBIDAE)
Г. X. Франк и A. X. Мейлинт
Раковина у Biomphalaria pfeifferi имеет Форму логарифмической
спирали, как и многих моллюсков и ее действительная Форма близка гео-
метрической. Чтобы вычислить ее поверхность и вес на квадратный мили-
метр, были использованы уравнения, основанные на этом факте. Вычисле-
ния, сделанные прямым путем для проверки этого факта, в общем были со-
гласны с первыми. Результаты этих вычислений, основанные на естествен-
ных и искуственных популяциях, указывают, что средний их вес на квадрат-
ный милиметр увеличивается с возрастом и с увеличением в них количества
растворимого кальция. Вероятно это увеличение происходит в одинаковой
пропорции во всех частях раковины, Т.е. вес каждой части на кв. мм. при-
близительно равен среднему размеру всей раковины. По всей вероятности,
величина К. (радиус оборота / радиус спирали в той точке), или подобная
тому пропорция; высота раковины к максимальному ее диаметру, уменьшается
с возрастом и накоплением углекислоты в окружающей среде. Если ракови-
на у вида B.pfeifferi всегда близка к идеально геометрической форме,
как то подсказывает настоящее ограниченное исследование, то привычная
детальная конхометрия станет ненужной. Если будет найдено, что скорость
удаления от центра (3) и диаметр устья (относящийся к ?) в группах оди-
накового размера значительно отличаются, то только полный математичес-
кий анализ будет достаточным.
466 MALACOLOGIA
ABCTPAKT
РЕПРОДУКТИВНЫЕ ФУНКЦИИ И ФИЛОГЕНИЯ ЗАДНЕЖАБЕРНЫХ БРЮХОНОГИХ
МОЛЛЮСКОВ
Михаил Т. Гизлин
Чтобы дать более особенную базу для Филогенетических исследований,
сравнительная и Функциональная анатомия репродуктивной системы была кри-
тически рассмотрена у всего подкласса заднежаберных моллюсков. Новые
наблюдения были соединены с детальным обсуждением прежних работ. Особое
внимание уделено возможности найти Функциональные объяснения для морфо-
логических и физиологических вариантов, чтобы предложить филогенетичес-
кую теорию, как основу, которая до сих пор имела случайный характер.
При функциональном анализе особенности конвергенционного характера были
опущены и особое внимание было уделено сравнению, основанному на комплекс
фуекциональных дивергенций.
Детально рассмотрены гомологии отдельных частей репродуктивного
трактаи предложены некоторые изменения в систематике. Образование яич-
ных масс и гомологии желез их выделяющих обсуждаются и выясняются на ос-
новании гистологических, химических и эспериментальных наблюдений.
Обсуждены возможные причины эволюционных изменений. Функциональные
затруднения предков из за нераздельного полового протока были устранены
различными путями и эти дивергенции составляют основу для предполагае-
мых кладов, которые расцениваются другими данными.
В настоящей работе были приняты во внимание и прежние работы, коли-
чество хромосом, образ питания и другие особенности пищеварительной си-
стемы, как и морфология сперматозоидов, как добавочный признак при обсуж-
дении филогенетических проблем. При критическом рассмотрении паралле-
лизма или конвергенции, были приняты во внимание филогенетические до-
воды. ,
Система органов размножения семейства Onchidiidae указывает Ha
родственность легочным. Семейство Acteonidae имеет измененную систе-
му органов размножения и оно является родственным большинству других
заднежаберных; однако его репродуктивная система и другие особенности
указывают на его близкое родство семейству Hydatinidae; гистология Te-
нитальной ампулы допускает возможное родство роду Acoela. Предпо-
сылки, на основании которых предполагалось бифилетичное происхождение
крылоногих моллюсков, признаны негодными; монофилетичное происхождение
их согласуется с морфологией системы репродуктивных органов; морфология
сперматозоидов обеих групп напоминает таковые у Anaspidea и Sacoglossa.
Репродуктивные системы у Anaspidea, Sacoglossa, Diaphanidae и Cylindrobullidae
можно сравнить с предлогаемым общим предком с раздельным половым прото-
ком и предложить, что они все родственны. Семейства Retusidae,
Philinoglossidae, Bullidae, Atyidae n Runcinidae могут быть сгруппирова-
ны вместе на основании строения UX совокупительного аппарата, который
откладывает сперму и выделяет сперматофоры; у траввоядных родов этой
группы имеется пищеводный дивертикул и также сходства в строении желудка.
Взаимозависимость между личиночными стадиями ракушечных и триаулитическими.
В сверхсемействе голожаберных, аэолидация указывает на необходимость
пересмотра их систематики. Это исследование подтверждает естественную
классификацию многих групп.
MALACOLOGIA 467
ABCTPAKT
FONTELICELLA (PROSOBRANCHIA: HYDROBIDAE)
НОВЫЙ РОД 3AMANHO- АМЕРИКАНСКИХ ПРЕСНОВОДНЫХ УЛИТОК
ВОО Е jipsrt mu Ne BIMESAIGE
Fontelicella, gen. nov. (подсемейства Hydrobiinae ) состоит из
3-х подродов: Fontelicella s. s. (тип Fontelicella californiensis sp.
nov.) C 8 видами oT Плиоцена до настоящего времени, в западных
США и Нижней Калифорнии, Мексике, Natricola, subg. nov. (тип Poma-
tiopsis robusta Walker, 1908) с 3 видами в бассейне Снэйк Ривер в
штатах Айдаго и Вайоминг, США, и Microamnicola, subg. nov. (тип Amnicola
micrococcus Pilsbry, 1893), с 1 видом, живущим в бассейне реки Amap-
госса, в южной части штата Невада и в южной Калифорнии, США. Между хо-
polo описанными видами, ближайшим является Cincinnatia integra (Say),
живущая в восточных штатах США, этот вид отличается OT остальных строе-
нием совокупительного органа, пигментацией тела, Формой раковины и ноги.
Между описанными особенностями видов Fontelicella являются общая Dop-
ма, спосб передвижения, поведение, пигментация, наружная морфология, ра-
дула, семепровод, яйца и экология. Устройство меланина и зерен в облас-
ти головы, является особенно полезным указателем видовых характеристик,
на которые не было обращено должного внимания в предыдущих работах об
этом семействе.
АБСТРАКТ
АРКТИЧЕСКИЙ РОД МУА
Дан Ларсон
Настоящий доклад имеет целью внести ясность в ошибочное представ-
ление об арктическом роде Муа. Дженсен (1900) указал (на датском языке),
что все тогдашние сведения о виде Myaarenaria Linnaeus из Арктики
были ошибочны и относились Фактически к виду Mya truncata Linnaeus,
который он назвал М. ovata. Самая надежная отличительная черта между эти-
ми двумя почти одинаковыми раковинами заключается в хрящевой пластинке
левой створки и в соответствующей ямке правой створки. Так как работа
Дженсена не является широко известной среди говорящего по английски ми-
pa, то северный вид Mya атепата до сих пор продолжает упоминаться из
Арктики. Позже Шлеш (1931) условно повысил форму М. ovata (которую сам
Дженсен считал заслуживающей полпжения не выше подвида) до положения ви-
да под именем М. pseudoarenaria, которым не следует пользоваться.
В этой работе даны ареалы живущих и вымерших трех Форм вида,
М. truncata: M. truncata forma typica, Linnaeus, М. truncata forma uddevallensis Forbes
и М. truncata forma ovata Jensen, a также и ареал вида М. arenaria,
насколько это удалось установить. Эти списки не полны. Исследователей,
работающих с видом Mya truncata, убедительно просят добыть больше дан-
ных о его формах в будущих работах.
Некоторые из новых свидательств о виде M. атепата из полярного круга,
тут обсуждены, во всех случаях они относятся к виду М. truncata forma ovata.
468 MALACOLOGIA
ABCTPAKT
ЭВОЛЮЦИОННЫЕ И СИСТЕМАТИЧЕСКИЕ ПРОБЛЕМЫ ПРОМЕЖУТОЧНЫХ ЛЮЦИНОИДНЫХ
ДВУСТВОРЧАТЫХ
А. Ли МкАлистер
Стратиграфические и морфологические данные указывают, что редкая
ордовикская двустворчатая раковина Babinka является иереходным звеном
между хвустворчатыми сверхсемейства Lucinacea и некоторыми их предка-
ми, напоминающими моноплакофоры. Данные палеонтологии и исследования
функций живущих видов указывают, что возможно, что надсемейства
Lucinacea, Leptonacea и род Babinka являются отдельной эволюционной вет-
BEN, сохранив - особые адаптивные признаки с ранней палеозойской эры.
Эту ветвь, вероятно, следует рассматривать, как отдельную систематичес-
кую группу (таксон), высокого развития. МЛюциноиды, очевидно, не дали
от себя какую нибудь другую группу двустворчатых и, по всей вероятности,
не родственны ни одной из таксодонтных групп, с которыми они обычно
обобщаются. Совершенно независимое происхождение люциноидных двуствор-
ватых подсказывает, что Bivalvia суть полифилетического происхождения
от недвустворчатых моллюсков.
АБСТРАКТ
ФУНКЦИОНИРОВАНИЕ СТАТОЦИСТОВ У ПРЕСНОВОДНОЙ УЛИТКИ
РОМАСЕА PALUDOSA (AMPULIRIDAE)
Андрей МакКлейри
Две группы улиток были исследованы. В группе 1 было 15 улиток, y
которых был удален левый статоцист, 15 улиток, у которых статоцист был
обнажен, но не удален, и 15 - контрольных нетронутых. В группе Il, было
8 улиток, у которых были удалены оба статоциста, 8 улиток с обнаженным
статоцистом с обеих сторон, и 8 - контрольных. Перед операцией улитки
были анастеаированы погружением в раствор MS 222 (0.25 гр / литр), при-
близительно на час. Ранки были быстро закрыты и улитки стали активными
через час после операции. После вскрытия никаких признаков регенерации
обнаружено не было.
Следующие особенности поведения были исследованы: быстрота и на-
правление их движений, степень активности, положение тела при отдыхе,
способность вернуться к нормальному положению, после того как животное
было перевернуто, ресничное питание и поверхностное дыхание.
Во время этих исследований, у некоторых особей из группы П, как
оперированных, так и надрезанных, появился ненормальный прогиб в рако-
вине. Наблюдения над степенью активности группы I, оперированных и
надрезанных улиток, показали, что они были менее активны и не могли от-
дыхать на вертикальной поверхности, как то делали улитки контрольные.
И те и другие признаки были признаны результатом операционных надрезов.
Наблюдения над активностью улиток группы П показали, что опери-
MALACOLOGIA 469
рованным улиткам было труднее оставаться на вертикальной поверхности,
чем тем, что были только надрезаны или контрольные; и это было понято
как результат удаления статоцистов.
За исключением вышеописанных наблюдений, значительной разницы меж-
ду поведением оперированных, надрезанных и контрольных не наблюдалось.
Улитки, у которых были удалены оба статоциста, не потеряли способ-
ности подниматься на поверхность воды для дыхания.
Между возможными факторами, регулирующими чувство направления вверх,
с удалением статоцистов, свет сверху и градиент кислорода, вероятно ан-
нулировали свет сбоку и циркуляцию воды. В границах описанных эксперимен-
тов, есть указания, что перемещение улитки не лишает ее способности дви-
гаться вверх. Есть также указания на градиент давления и плавучесть.
легких.
АБСТРАКТ
НЕКОТОРЫЕ ЗАДНЕЖАБЕРНЫЕ МОЛЛЮСКИ ИЗ МКРОНЕЗИИ
Эрнест Маркус
Коллекция из 130 заднежаберных моллсков из Микронезии, принадлежа-
щая Национальному музею США, содержит 53 вида. Только 10 видов являются
новыми и половина из них размерами не превышает 5 мм в длину. Эти нем-
ногие экземпляры отличаются однобразием фауны коралловых рифов западного
Великого океана, большинство же более крупных видов уже известно. Опи-
саны следующие новые виды: Stiliger (Ercolania) illus, Elysia bayeri, Elysia тата,
Hypselodoris cuis, Discodoris lora, Discodoris ylva, Catriona lonca, Catriona
urquisa, Noumeaella rehderi и Muessa evelinae генотип нового pola ce-
мейства Favorinidae, родственного роду Herviella.
ABCTPAKT
МОРСКИЕ БРЮХОНОГИЕ МОЛЛЮСКИ ПОДКЛАССА EUTHYNEURA ИЗ АТОЛЛА
ЗНИВЕТОК ЗАПАДНОЙ ЧАСТИ ВЕЛИКОГО ОКЕАНА
Э. Марку и Иван Б. Бёрч
Настоящая работа является следствием изучения морских моллюсков
подкласса Euthyneura, собранных вторым автором на атолле Эниветок,
группы Маршаловых островов, в Феврале - Апреле 1960 года. Было собрано
17 видов, из которых 5 описаны в настоящей работе, как новые виды:
Haminoea тизейа, H. linda, Chromodoris briqua, Herviella mietta и Onchidella evelinae.
Из остальных 12 видов 7 распространены к востоку от западной части Ин-
дейского океана (2 из них также находятся в Красном море) от этого атол-
Ja , 2 вида являются общетропическими или общеподтропическими, 2 вида
470 | MALACOLOGIA
известны исключительно только в западной части Великого океана. Срав-
нительная однородность фауны рифов западного Индопасифика видна из Pak-
та, 9 видов (т.е. более 50 процентов) из общего числа известны от за-
падного края Индийского океана и до середины Великого. Род Herviella,
повидимому, ограничен распространением только в западной части Великого
океана. Замечательными являются рецидивная вентральная конечность ноч-
ки и оболочка стилета в дивертикуле пенисного мешка у Onchidella.
в районе Австралии, Новой Зеландии и прилежащих осровах.
АБСТРАКТ
ЭКОЛОГИЯ CYRTODARIA SILIQUA И ИСТОРИЯ ЖИЗНИ РОДА CYRTODARIA
(BIVALVIA: HIATELLIDAE)
Во Hr Sana
Cyrtodaria siliqua (Spengler) распространена от северного края
отмелей острова Большого Ньюфаундленд и до отмелей Джорджа, она Bcpeua-
ется на дне из мелкого песка, на глубине в 500 м, но главным образом, на
глубинах от 50 и ло 150 м, а также и на глубинах более 250 м, но только
там, где находится сильный приток воды направленный вниз, она наблюда-
лась при температурах от -1.0 и до +5.7 и при солености от 32.3 и до
34.2 процентов.
Этот подвижной вид питается планктоном, находящемся в суспензии и
предпочитает рыхлое дно. Способ его питания определяет глубину и харак-
тер субстрата. Вероятно он не может размножаться при постоянной низкой
температуре, почему он не распространяется на север от отмелей Ньюфаунд-
ленда. По своему ареалу С. siliqua - западно-атлантический северный
вид, а по температурным требованиями, он относится к нижне-арктической
северной фауне.
Род Cyrtodaria Daudin атлантического происхождения. Он образо-
вался в промежуточный период между Палеогеном и Неогеном, а предки его,
возможно, жили в морях Южно-Прусской геосинклинали в Палеогене: к концу
Неогена они распространились по мелям Северного Атлантического океана и
Арктики и разбились на несколько родственных видов. Благодаря пост-пли-
осеновому оледенению, эти виды вымерли по берегам Европы и в западном
Атлантическом океане. С. siliqua была оттеснена на юг. После ледни-
кового периода, она распространилась на северо-запад до Гренландии, но
из за больших глубин у проливов Дании, она не смогла продвинуться до
Исландии, где она обитала ранее, в доледниковое время (Нэзис, 1961).
С. kurriana - другой живущий вид этого рода является циркумполярным ви-
дом, обитающим исключительно в солоноватых прибрежных отмелях, он берет
свое начало в Арктике в начале Плеистоцена. Его предки предпочитали бо-
лее теплую воду нормальной солености. Благодаря повторным высыханиям
мелей во время эвстатических регресий, он был отеснен в соленоватые воды.
В насале после-ледникового периода, или же в межледниковое время, он
мигрировал к югу, до устья реки Амура, но после потепления и повышения
солености в прибрежных водах дальневосточных морей, он там вымер. Настоя-
MALACOLOGIA 471
mee потепление Баренцева моря может еще сократить ареал этого вида.
Род Cyrtodaria указывает Ha 2 главных тенденции видообразования:
"линейную или цепную" и "букетную", типа Е.Ф. (по Гурджановой, 1951 г.).
Эволюция этого рода по "линейному" типу привела в результате к транс-
формации предков, требовавших более высокие температуры (сравнительно
редкий случай арктического вида Атлантики) в арктический вид
С. Rurriana, где каждый вид цепи сохранил морфофизиологическую адаптацию к
определенному типу питания.
АБСТРАКТ
ХРОМОСОМНЫЕ ЦИКЛЫ У НАЗЕМНОЙ УЛИТКИ CATINELLA VERMETA
(STYLOMMATOPHORA: SUCCINEIDAE)
С. М. Паттерсон и Иван B. Бёрч
Между стебельчатоглазыми рода Catinella по крайней мере три вида
отличаются от остальных малым количеством хромосов Catinella rotundata
с Гавайских островов, n=5 (2n=10); С. vermeta и С. texana, п=6 (2n=12).
С. vermeta в особенности заслуживает исследования хромосомных циклов
ее сперматогенезиса, из за малого количества хромосом и их большой вели-
чины.
В общем циклы ее не отличаются от таковых у других животных и особен-
но напоминают циклы, наблюдаемые у подкласса Euthyneura. Но детали
развития гораздо заметнее, и различные стадии его легко отличимы и те,
что не были выяснены ранее, стали вполне ясными. Детальное описание
хромосомных циклов У С. vermeta дает ясное представление о мейотическом
процессе у этой группы брюхоногих и значительно расширяет сведения, дан-
ные в предыдущих работах.
Ранние мейотические хромосомы выглядят пушистыми, распространяют
нити, затвердевающие в промежуточные профазные хромосомы, ясно обозна-
ченной сиральной формы; центромеры выглядят как слегка окрашенные и не-
окрашенные пятна. Следующее уплотнение делает метафазные хромосомы гуще
окрашенными, они образуют гладкие края и центромеры обозначатся только
сжатием. Анафазные хромосомы похожи на них, но они меньше размерами.
Первое мейотическое профазное ядро образуется после последнего пред-
мейотического деления. Лептотенные хромосомы выглядят как длинные, OT-
дельные нити, слегка окрашенные с хромомерами во всю их длину. Свобод-
ные их концы указывают на поляризацию, характерную для "букетной стадии".
Парование зиготен начинается у поляризованных концов и выглядит как хро-
момер за хромомером соединяются по длине гомологичных нитей. XPOMOCOM-
ные пахитены короче и гуще окрашены. Гомологи начинают "отталкивать"
друг друга, образуя разделения по линии ранних диплотен хромосомов. По
мере развития диплонемы, хромосомы рассеиваются и выглядят слабо окра-
шенными. Хиазмы стремятся к концам нитей и уплотнение продолжается, ког-
да хромосомы образуют кольца, палочки и кресты или же светлые петлевид-
ные фигуры, характерные для диакинеза. В метафазе I биваленты образуют
плотное кольцо, дугу или фигуру вроде палочки. Гомологичные центромеры,
со своими хроматидами разделяются в стадии анафаз I, образуя сдвоенные
472 | МАГАСОГОСТА
хромосомы (диады), приблизительно вдвое меньше чем в метафазе I, бива-
ленты. Во время последующего далее цитокинеза, хромосомы начинают вто-
рое мейотическое деление без заметного периода интеркинеза.
Диады прометафазы Il, прежде чем выстроиться в экваториальном
плане, напоминают позние хромосомы метафазы II, толвко сильно сжаты и
густо окрашенные, в форме "гантели". Во время анафазы П, каждый диаи
отделяется и образует две гонады, которые движутся к противоположным по-
люсам, где начинается телофаза Il, после Aero следует цитокинез.
Молодые сперматиды образуются после, каждая с заметной ядерной оболочкой.
В период спермиогенеза хроматин разлагается и уплотненное ядро превра-
щается в зрелого сперматозоида.
АБСТРАКТ
РОСТ И ЕГО ЗАМЕДЛЕНИЕ У ONCOMELANIA
| (GASTROPODA: HYDROBIIDAE)
Генрих ван дер llano и Георгий М. Дэйвис
Эти данные относятся к проблеме быстрого и аккуратного выращивания
лабораторным путем в больших количествах моллюсков вида Oncomelania для
исполвзования их при изучении паразита Schistosoma japonicum . Предыду-
щие работы указывают на скорость роста этих улиток, достигнутую в других
лабораториях - от 0.3 до O. 4 мм в неделю, где их смертность в одном слу-
чае достигала 38 процентов.
Описанный тут способ’ выращивания культуры дает регулярный рост в
0.65 мм в неделю со смертностью ниже 10 процентов. Самый быстрый рост
получается когда 1 или 2 улитки, только-что вылупившиеся из яйца (в 2.0
или 2.5 оборота), помещаются в блюдце Пэтри диаметром в 9 см. В центре
блюдца помещается лепешка из алкалического нестерилизованного пресновод-
ного ила с нормальным содержанием диатомовой водоросли. Прибавив воды,
блюдце прикрывают и ставят под лампу в 150 футо-свечей на 10 - 12 часов
в сутки. Без прибавки питания, температура поддерживается в 25, - 2 гра-
дуса (по Цельсию).
Когда число улиток в каждой культуре было увеличено до 5 и до 10,
в результате были получены карликовые формы, т.е. заметное замедление и
в их росте и развитии. В соответствии с замедлением роста наблюдалось и
замедление в развитии гонад, отсутствие развития половых органов и повы-
шенная смертность. Так как наружно карликовая раковина не отлична от
нормальной, то ее можно опознать только зная ее возраст.
Максимальный рост улитки зависит от суммы следующих данных: свет,
достаточный объем сосуда подходящая почва со здоровой микрофауной.
Самыми критическими требованиями успешной культуры являются постоянство }
в свете и размер сосуда, ил с высоким содержанием кальция и способный nu"
тать обильную микрофауну зеленых и диатомовых водорослей. {
MALACOLOGIA 473
ABCTPAKT
СРАВНИТЕЛЬНОЕ ИССЛЕДОВАНИЕ ПИЩЕВАРИТЕЛЬНОГО ПРОЦЕССА У
БРЮХОНОГИХ DRUPA RICINA И MORULA GRANULATA
Ши - Квей By
На Гавайских островах среди пышной растительности морских водорос-
лей, вместе с голотуриями и губками, встречается брюхоногий моллюск
Drupa vicina (L.) В сообществе с двустворчатым моллюском Isognomon,
губками и меньшим количеством водорослей встречается другой брюхоногий
хищный моллюск Morula granulata (Duclos).
Описывается анатомия и гистология пищеварительной системы y D. ricina
сравнительно с таковым у М. granulata. В общем они довольно сходны, 34
исключением радулы, комплекса кишечника, желудка и ректальной железы.
У D. vicina радула имеет 5 зубцов без полого основания, а М. granulata
имеет радулу с 3 зубцами и полое основание в центре. Это значительное
различие находится в тесной связи с комплексом желез и кишечника: у D.
vicina 2 симметрично развытые вспомогательные железы совершенно свобод-
ны от главной их массы, ау М. granulata большая из слюнных желез це-
ликом погружена в массе остальных, а правая поменьше размерами остается
свободной. Желудки обоих видов в общем имеют вид подковообразного меш-
ка, но желудок D. vicina снабжен дивертикулой со стороны пищевода, а
желудок М. granulata таковой не имеет. Ректальная железа у D. ricina
желтого цвета и неопределенных очертаний, ау М. granulata она черна и
легко отличима по внешнему виду.
Обсуждены Функциональные аспекты пищеварительной системы обоих ви-
дов. Во время питания, ротовое отверстие, слюнные и вспомогательные же-
лезы смачиваются совместно. За исключением ротового отверстия ресничные
волны проходят через всю систему пищеварения.
Наблюдалось, что Morula может сверлить двустворчатые, но предпо-
читает падаль, а Drupa, не считается типичным хищником моллюсков с
жесткой раковиной, но питается живыми губками, голотуриями и падалью.
Манера питания и разница в диете находятся в связи с различиями в строе-
нии пищеварительной системы. Сравнение методов питания и структуры же-
лудков у этих видов с теми же особенностями у других хищных месогастро-
под, возможно, что указывает на принадлежность Drupa и Morula к ca-
мым основным и примитивным группам стеноглоссовых, отражая их происхож-
дение от месоглоссовых предков.
ik
MALACOLOGIA 475
ERRATA
MALACOLOGIA regrets the occurrence of a number of errors and inconsistencies in
the first article of Vol. 3 (Dazo, B. C., p 1-80). The more important of these, in
particular irregularities relating to figures, tablesor numbers, are herewith corrected.
p 12, left column, 4th paragraph, line 3: “Table 12” should. read
“Table 13”. 5thparagraph: “Table 13” should read “Table 14”.
p 21, left column, 3rd paragraph, under Eyes, line 4: delete “Text
Figure 5” and substitute “PLATE Ш, Fig. 1; Text Figure 7”;
right column, 2nd paragraph, under Tentacles, line 6: instead of
“Text Figure 5” read “PLATE Ш, Fig. 1 and Text Figure 7”.
р 23, PLATE Il: The upper left unnumbered figure is Fig. 1.
р 27, PLATE Ш: The center unnumbered figure ofthe complete snail
is Fig. 1. In Fig. 4, “crystalline roa” should read ”crystalline
rod”:
р 28, left column, line 9: “PLATE IV” should read “PLATE Ш”.
p 29, left column, 2nd paragraph, line 6: “Figure 8(1)” should read
“PLATE VI, Fig. 1”.
right column, 2nd paragraph, line 2: insert “a” to read “ ...
surrounded by a bell-shaped . . .”
p 30, left column, 2nd paragraph, last line: “Figure 8(6)” should
read “PLATE II, Fig. 1; PLATE VI, Fig. 5”. Last paragraph,
lines 1 and 2: “Figure 8(1)” should read “PLATE VI, Fig. 1”.
p 31, right column, line 2: “later teeth” should read “lateral teeth”.
p 32, FIG. 6: The upper unnumbered set of jaws and radular teeth is
1. The jaws and radular teeth of both species are drawn to
the same scale.
right column, last paragraph, line 2: “PLATE VII” should read
“PLATE VI”.
p 34, right column, line 5: “Figure 8(2)” should read “Fig. 8(4)”.
p 39, PLATE IV: The unnumbered figure on the left is Fig. 1. The
legends are incorrect and should read:
FIG. 1. Male reproductive system of Goniobasis livescens. 28X.
FIG. 2. Female reproductive system of Goniobasis livescens.
28X.
FIG. 3. Typical, eupyrene spermatozoon, similar to that of
Goniobasis laqueata illustrated by Woodard (1935).
FIG. 4. Upper portion of a mature apyrene (atypical) spermato-
zoon drawn from a fresh smear preparation. 3570X.
FIG. 5. Crescent-shaped spermatophore with its tapering ends.
53X.
p 40, left column, 4th paragraph: “p 137-146” should read “p 55-60”.
p 50, TABLE 6, Footnote 18: “p 88” should read “p 35-36”.
р 52, FIG. 11: The magnification (not given) of all shells is .82X.
476
p 54,
p 57,
p 60,
p 61,
p 62,
MALACOLOGIA
PLATE V: The legends should read:
FIGS. 1 & 2. The egg masses of Pleurocera acuta.
FIG. 1. Drawing of detached egg masses of various shapes;
some are turned over showing the underside of the mass
with exposed eggs. 13X.
FIG. 2. Drawing of recently laid egg clutch with embryos in
the second cellular division as seen by transmitted light.
The opaqueness of the embryos makes them appear black.
30X.
FIGS. 3 & 4. The eggs of Goniobasis livescens.
FIG. 3. Drawing of 2 detached eggs on their substratum. 25X.
FIG. 4. Drawing of newly laideggwith its adhering covering
of soil as seen by transmitted light. The opaqueness of
the egg makes it appear black. 60X.
right column, lines 7-8: “Rows for lines) of 2-3 eggs were
likewise noted”, should read: “Rows (or lines) of 2-3 eggs
were likewise noted;” second paragraph, last line: “p 172”
should read “p 73”.
left column, line 11: “in 256 days” should read “in 26 days”.
right column, 15 paragraph, last line: for “serching” read
“searching”; last paragraph, last line: instead of “0.27-3.87
mm” read “0.27-3.82 mm”.
left column, line 15: “p 144” should read “p 57”.
TABLE 11: 154 line under the heading Number of Whorls:
“1-10” should read “1”.
PLATE VI: The legend to Fig. 4 should read: “Longitudinal
section of the mantel region, showing cross-sections of the
gill filaments (G). The large intestine (I) appears on the lower
right corner. Approx. 30X.
PLATE VII: The legend should read: “Histological sections of
Goniobasis livescens”.
TABLE 16: “Plagioporus sinissini huroni” should read “Plagio-
porus sinitsini huroni”.
nr } |
ры hi ren И
М BOUND SEPT 1979
ET
3 2044 072 160 2