J. Moll Stud. (1997), 63,353-367
© The Malacological Society of London 1997
HOMOLOGY OF THE PALLIAL AND PULMONARY CAVITY
OF GASTROPODS
BERNHARD RUTHENSTEINER
Zoologische Staatssammlung Milnchen, Miinchhausenstrasse 21, D-81247 MUnchen, Germany
gastropods. Predominantly terrestrial and fresh
water forms with direct development were
The development and morphology of the paJlial and
studied, because of their relative ease of culture
pulmonary cavities of various gastropods has been
and obtaining the developmental stages.
investigated using epoxy-resin serial sections. In the
Reports of lung (=lung cavity or pulmonary
veliger larvae of Cellana sandwicensis (Patellogastrocavity)
development led to the interpretation
poda), Gibbula adansonii (Vetigastropoda), Modulus tectum (Caenogastropoda) and Ovatella myosotis that this organ is a secondarily invaginated,
newly acquired structure of pulmonates.
(Pulmonata) the formation of the pallia! cavity is
Accordingly, it has been considered to be nonnearly identical. After shell formation a shallow
homologous with the prosobranch pallial
dorsal pallial groove develops beneath the mantle
edge. During the late veliger stage, the ectoderm
(=mantle) cavity (Fol, 1880; Regondaud, 1964;
forms a deep invagination along the bottom of the
Cumin, 1972; Meisenheimer, 1898; Heyder,
pallial groove on the right side of the larva, giving
1909; Ghose, 1963; Moor, 1977). Consequently,
rise to the pallial cavity. In the ellobiid O. myosotis authors working on morphology have regarded
the pallial cavity becomes the lung (=pulmonary
the pallial cavity and the lung to be two differcavity), without any major post-metamorphic modifient or separate structures that may be present
cation. Thus, the lung of this species is clearly
in a single individual (e.g. Climo, 1980; Tillier &
homologous with the pallial cavity of prosobranchs.
Ponder, 1992). The elaboration of a lung has
The lung of pulmonates with veliger development,
been regarded as a synapomorphic character
as well as of fresh water basommatophorans and
stylommatophorans, can be shown to be homologous
of pulmonates in many phylogenetic studies
by comparison of adult morphology. In contrast to
(e.g. Salvini-Plawen, 1991; Nordsiek, 1992;
previous views, the pulmonate lung should be
Salvini-Plawen & Steiner, 1995). Other authors,
regarded as truly homologous with the pallial cavity
however, appear completely unaffected by
of prosobranchs and opisthobranchs. In the
embryological arguments and regard the pulonchidiid pulmonate Onchidium cf. branchiferum,
monate lung cavity as the pallial cavity (e.g.
the larval pallial cavity shifts posteriorly after metaMorton, 1988). The fact that primitive pulmorphosis, where it gives rise to a lung and a cloaca.
monate lungs resemble pallial cavities in many
Contrary to previous interpretations, it can be shown
ways has prompted a minority of authors
that the onchidiid lung is homologous with at least
part of the pallial cavity. Smeagol climoi has only a
(Fretter, 1975; Brace, 1983) to argue against
small pallial cavity and no separate lung. The prethe secondary derivation hypothesis. They
viously described 'lung' is shown to be a gland. The reasoned that the interpretation of lung
re-evaluation of the development and morphology
development in direct developers may be misof the pulmonate lung has important systematic
leading, since the organisation of developmental
implications: (1) The pulmonary cavity does not repstages
may be altered in large, yolk-rich eggs.
resent a synapomorphic character of pulmonates. (2)
ABSTRACT
The gymnomorphs cannot be separated from the
remaining pulmonates based on lung development.
(3) The lack of a lung in the smeagolids might give
reason to reconsider this group's systematic placement within the pulmonates.
INTRODUCTION
Until recently, pulmonates were the main subjects for morphogenetic investigations among
The development of a primitive pulmonate
such as Ovatella myosotis, which has indirect
development and passes through a veliger
larval stage, may be informative in this matter.
Comparisons with pallial cavity formation in
prosobranchs, which also have indirect development and a veliger stage, may be important to
interpreting lung development in pulmonates.
As there is little information presently available
in the literature, a re-examination of such
species is necessary.
354
B. RUTHENSTEINER
The systematic placement of two slugshaped groups (onchidiids and smeagolids) has
been strongly influenced by the interpretation
of their pallial complex. In onchidiids a developmental study may shed light on the homology of this group's lung with that of other
pulmonates, while a re-examination of the
smeagolid 'lung' appears necessary after Tillier
& Ponder (1992) questioned the previous
interpretation of that organ.
In the text that follows, traditional names
have been applied to higher systematic groups,
as these are well known and appropriate for
the topics discussed here. These include paraphyletic groups (e.g. prosobranchs) which are
not specifically marked as such.
of Houghton Bay, Wellington, New Zealand were
provided by the Australian Museum, Sydney.
Development stages of all species investigated
were fixed in Bouin's fixative. Additionally some
species were fixed in buffered glutaraldehyde (M.
tectum, Onchidium cf. branchiferum) or buffered
glutaraldehyde followed by osmium postfixation (C.
sandwicensis, M. tectum, Onchidium cf. branchiferum). Dehydration in a graded series of ethanol
preceded embedding in Araldite or Spurr's resin.
Ribboned serial sections with a thickness of 1.5 or
2.0 u,m were prepared by putting contact cement on
the underside of the block. Reconstructions were
made by measuring distances on sections with the
help of an ocular micrometer on a microscope.
RESULTS
MATERIAL AND METHODS
Adult specimens of the patellogastropod Cellana
sandwicensis (Pease, 1861) (Patellidae) were collected next to Diamond Head, Honolulu, Hawaii.
Artificial fertilisation and egg maturation was
carried out after gonad excision, as described by
Corpuz (1981). Developmental stages of the
vetigastropod Gibbula adansonii (Payraudeau, 1826)
(Trochidae) were obtained from egg masses laid on
the glass walls of an aquarium by specimens collected in the northern Adriatic Sea. Developmental
stages of the cerithioid caenogastropod Modulus tectum (Gmelin, 1791) (Modulidae) were derived from
egg masses deposited by adults found in sea water
tanks of the Kewalo Marine Laboratory, Honolulu,
Hawaii. Adults of the pulmonate Ovatella myosotis
(Draparnaud, 1801) (Ellobiidae) were collected near
Alberoni at the Lido di Venezia, Italy, and maintained in porous flower pots. Development stages
were obtained from egg masses deposited within
these pots. Adult specimens of the pulmonate
Onchidium cf. branchiferum (Onchidiidae) were
collected from boulders at the inner side of the reef
in front of Ala Moana Beach, Honolulu, Hawaii.
They were kept among rocks in a table with running
sea water. Larvae were obtained from egg masses
deposited on the underside of the rocks. The planktonic larval stages of C. sandwicensis, M. tectum and
O. cf. branchiferum were kept in milh'pore filtered
sea-water in airlift-droplet stirrer vessels (Strathmann, 1987). Antibiotics were added to cultures of
C. sandwicensis and M. tectum to minimise bacterial
infection. Larvae of M. tectum and O. cf.
branchiferum were fed with monocellular algae.
Metamorphosis could be induced in Onchidium cf.
branchiferum by placingfield-collectedrocks covered
with the slime of adult individuals in the larval cultures. These rocks subsequently served as substratum
for inter- and post-metamorphic stages. Formaldehyde fixed specimens of Smeagol climoi Tillier &
Ponder, 1992 (Smeagolidae), collected at the east end
Larval pallial cavity
Gibbula adansonii, Cellana sandwicensis, Modulus tectum and Ovatella myosotis all have the
following processes in common during the
development of the pallial cavity: As a result
of shell and mantle formation, the mantle
margin partly protrudes above the body
surface and thus encloses a space, the pallial
groove (Figs. 6B, 10B, 11B, PR), underneath.
This groove is most prominently developed
dorsally and laterally to the head portion of
the larvae. When formation of the pallial
groove is completed, an invagination of thickened epithelium appears along its innermost
portion on the right side of the larva. This
invagination deepens and gives rise to a large
pallial cavity.
Cellana sandwicensis develops rapidly without the protection of an egg-capsule. The
pallial cavity forms in the veliger larva of this
species about 20 hours after fertilisation (Fig.
1), at the end of the torsion process. The pallial
cavity continues to deepen until three days
after fertilisation, by which time the pallial
cavity extends to the terminal tip of the visceral mass. Figure 2 shows a fully developed
pallial cavity. The anus opens deep within the
pallial cavity, along its right side. The two
kidneys lie adjacent to the pallial cavity epithelium, one on either side of the hindgut. The
larva] pallial cavity contains three ciliated
areas: one lies deep within the cavity, on the
right side in the anal area; two broad, opposed
ciliated tracts lie on the roof and floor of the
pallial cavity, extending towards the opening
on the left side; the third area consists of a
small ciliated field in the roof on the right side
of the pallial cavity.
355
HOMOLOGY OF PALLIAL AND PULMONARY CAVITIES
Gibbula adansonii undergoes development to the posterior extension on the left side.
and metamorphosis within an egg-capsule and When fully developed in the larva, the position
hatches as a crawling juvenile. Invagination of
and relative size of the pallial cavity are the
the pallial cavity begins at the age of two days same as those of the pulmonary cavity in the
(Figs 3, 6). The larval pallial cavity reaches its adult animal.
full size in the four day old larva (Figs 4, 7).
The larval pallial cavity of Onchidium c.f.
Simultaneously with the invagination of the branchiferum is formed during the last quarter
pallial cavity, its opening, lying initially on the of the planktotrophic larval phase, which
right side, becomes greatly enlarged and requires at least 17 days to achieve metashifted until it lies directly dorsal to the head morphic competence. In the competent larva
(Fig. 7B). The fully developed palhal cavity (Fig. 16) the pallial cavity is voluminous and
extends backwards near the terminal tip of the fills the most terminal extension of the visceral
visceral mass. The anus and kidney lie within mass. The overall morphology is very similar
the pallial cavity along its right side. The rela- to that of Ovatella myosotis: pallial cavity
tive size and position of the pallial cavity opening, anus, kidney pore and osphradium
remains unchanged during metamorphosis. In have identical positions. The anterior end of
this species, there are two areas of ciliation the ciliary band lies deep within the pallial
within the mantle cavity: one band of cilia cavity, in contrast to that of Ovatella myosotis.
extends posteriorly into the cavity from the left
side of the mantle cavity opening, the other
Lung differentiation
band extends posteriorly from the middle of
the pallial cavity roof.
In Ovatella myosotis the pallial cavity, which
Modulus tectum hatches seven days after egg represents the future pulmonary cavity, underdeposition. The larvae are planktotrophic. goes only minor alterations during post-metaInvagination of the pallial cavity occurs five morphic development, which begins on day 15.
days after oviposition (Fig. 5). In the fully The ciliary band becomes reduced, the epideveloped larval pallial cavity, the anus lies thelium adjacent to the anus becomes strongly
anteriorly along the right side and the kidney ciliated and partly differentiated into the folded
pore lies deep within. Three ciliated areas are closure apparatus of the anus, and the opening
distinguishable in the mantle cavity: one con- of the pallial/pulmonary cavity becomes
sists of two opposed tracts that lie on the roof gradually reduced in size relative to the
and floor of the pallial cavity, extending pos- animal's total size. Musclefibersbecome differteriorly from the right side of the mantle cavity entiated in the surrounding tissue to allow
opening; a second area comprises a small band closure of the pneumostome. The differentiaof cilia that extends posteriorly from the tion of the respiratory lung epithelium begins
middle of the mantle cavity roof; the third after metamorphosis, when the 'vena pulconsists of a small ciliated field on the right monalis' first appears in the (future) lung roof.
side near the anus.
Components of the developing reproductive
Ovatella myosotis develops within the egg- system begin to differentiate on the ventral
capsule where it undergoes a veliger stage. The epithelium of the lung several weeks after
pallial groove is fully developed nine days after hatching, when the shell length has reached 0.7
egg deposition. One to two days later, the mm. The bursa copulatrix together with the
pallial invagination appears at the bottom of duct and the anlage of the pallial glandular
this groove on its right side (Fig. 10). The portion of the gonoduct are first formed as
invagination process is completed by day 12 or grooves and subsequently constricted from this
13, and leads to a deep, voluminous pallial epithelium. The connection between the newly
cavity (Fig. 8) that extends posteriorly for two formed genital elements and the epithelium is
thirds of the visceral mass (Fig. 11). The pallial lost when shell length reaches 1.2 mm.
cavity opening remains on the right side
Metamorphosis of Onchidium c.f. branchithroughout invagination (Fig. 11B), although ferum consists of two stages. The first stage is
the most terminal extension lies on the left side characterized by settlement, followed by velar
of the larva (Fig. 11B). The anus lies within the loss and a creeping way of life. In the second
pallial cavity next to its opening. The kidney stage, a flat, slug-like morphology is achieved,
opens within the pallial cavity (Fig. 9), on its preceded by loss of shell and operculum (five
right side. An osphradium is represented by a to rune days after settlement). The pallial
ciliated ridge in the most dorso-anterior cavity is still present in the shelled, interregion. A ciliary band leads from the opening metamorphic phase (Fig. 12). In this stage both
356
B. RUTHENSTEINER
Figures 1-5. Micrographs of sections of prosobranch larvae. 1. Cellana sandwicensis. 20 hour old veliger;
transverse section. Scale bar = 30 y.m. 2. Cellana sandwicensis. Three day old veliger; transverse section. Scale
bar = 40 jim. 3. Gibbula adansonii. Two day old veliger; transverse section. Scale bar = 40 jim. 4. Gibbula
adansonii. Four day old veliger, transverse section. Scale bar = 40 |xm. 5. Modulus tectum. Five day old
veliger; transverse section. Scale bar = 40 u.m. Abbreviations: AN PC, anlage of pallial cavity; F, foot; FO,
foregut; HG, hindgut; ML, midgut gland; PC, pallial cavity, S, statocysts; V, velar lobes.
the volume and the opening of the pallial
cavity become gradually reduced in size, the
pallial opening moves posteriorly and slightly
to the right (Fig. 12, PO) due to detorsion of
the visceral mass. After the slug-like morphol-
ogy is achieved, the pallial cavity lies terminally (Fig. 17,19A), with the opening slightly to
the right of the midline. The highly complicated, differentiation process that follows is
illustrated in Figure 19. Around 11 days after
HOMOLOGY OF PALLIAL AND PULMONARY CAVITIES
357
AN PC
\
Figure 6. Gibbula adansonii. Two day old veliger (same specimen as Figure 3). A. Lateral view. B. Dorsal
view. Abbreviations: AN PC, anlage of pallial cavity, AN V, anlage of velar lobes; F, foot; O, operculum; PR,
pallial groove.
B
--y
Figure 7. Gibbula adansonii. Four day old veliger (same specimen as Figure 4). A. Lateral view. B. Dorsal
view. Abbreviations: F, foot; O, operculum; PC, pallial cavity, T, tentacles; V, velar lobes.
achieving the slug-like shape, that portion of
the pallial cavity lying anterior of the renal
pore becomes constricted from the remaining
pallial cavity (Figs. 18,19B, C). Thereafter, this
portion, the future lung, becomes increasingly
isolated, until the connection to the rest of the
pallial cavity consists only of a duct. This duct
separates from the tubular pallial cavity, its
opening moving towards the pallial cavity
opening (Figs 19C-E). Thirty-one days after
metamorphosis, the duct opening, the future
pneumostome, could first be observed opening
separately onto the body surface (Fig. 19F).
The remaining pallial cavity, the cloaca, represents a simple duct-like chamber leading from
the kidney and the hindgut (Figs. 13, 14, CL).
When the pulmonary duct is almost completely
separated from the cloaca, a tube-like portion
is constricted from the future lung. This constriction proceeds terminally over the whole
B. RUTHENSTEINER
358
8
/9 %
f
•
• ^
^
Figures 8-9. Ovatella myosotis. Sections of 13 day old veligers; 8. Midsagittal section. Scale bar = 60 jtm. 9.
Transverse section showing the kidney pore (arrow) opening into the pallial cavity. Scale bar = 20 \un.
Abbreviations: F, foot; FO, foregut; HG, hindgut; K, kidney; M, mouth; ML, midgut gland; PC, pallial cavity,
RS, radula sac.
AN PC
PR
5 0 (im
50(i m
Figure 10. Ovatella myosotis. 11 day old veliger. A. Lateral view. B. Dorsal view. Abbreviations: AN PC,
anlage of pallial cavity; F, foot; O, operculum; V, velar lobes.
length of lung and pulmonary duct (Fig. 19G),
and represents the anlage of the future genital
duct. This duct opens by a pore separate from the
cloacal opening and the pneumostome in the
adult animal (Fig. 19H). By the last develop-
mental stage observed (38 days post metamorphosis) the lung anlage is compressed and lies
adjacent to the kidney (Fig. 13,14, AN L). At this
stage, the animals had not made any attempts to
leave the water in which they were living.
HOMOLOGY OF PALLIAL AND PULMONARY CAVITIES
359
Figure 1L Ovalella myosotis. 13 day old veliger. A. Lateral view. B. Dorsal view. Abbreviations: AN T,
anlage of tentacles; F, foot; O, operculum; PC, pallial cavity; PR, pallial groove; V, velar lobes.
Morphology o/Smeagol climoi
The pallial cavity of S. climoi (Figs 20, 22) is
a symmetrical, medioterminal cavity with a
terminal, slit-like aperture. The cavity contains
three openings: the hindgut opens ventrally via
the anus; the kidney opens dorsally via a pore
(Fig. 22, KP); the large pallial gland opens via
a duct opening anterior to the kidney pore.
The epithelium of the pallial cavity consists of
tall, prismatic cells that are densely ciliated in
the area of the hindgut opening. Neither the
general anatomy nor the epithelial organisation indicate respiration as the main function
of the mantle cavity. Smeagol appears to
respire primarily through the entire body surface. This is indicated by the presence of a
dense net of voluminous blood sinuses lying
beneath the epithelium of the body surface.
The pallial gland (Figs 20, 22, PG, 21) lies
anterodorsally to the pallial cavity and has a
spherical overall shape. This gland consists of
many large cells, each containing a large
vacuole and a channel to the central duct (Fig.
21), which is connected to the pallial cavity.
DISCUSSION
Homology of lung and pallial cavity
The development of the lung in the ellobiid
Ovatella myosotis suggests that this cavity is
directly homologous with prosobranch and
opisthobranch pallial cavities. This contradicts
earlier opinions, which regarded the pulmonate lung as a newly acquired structure
unique to the pulmonates. There are two ways
to interpret these observations. Either (1) the
process of lung formation in O. myosotis differs fundamentally from that of fresh water
basommatophorans and stylommatophorans,
in which case these pulmonate lungs are not
homologous with ellobiid lungs, or (2) the lung
of O. myosotis is homologous with that of the
other pulmonates, and developmental processes in the latter were misinterpreted in
previous studies. The second hypothesis is
advocated herein.
Previous studies have interpreted the lung as
a secondary structure, but, as only pulmonates
with yolk-rich development were studied, the
significance of this interpretation is limited.
Direct development is a derived condition,
suppressing the development of a veliger larval
stage, and conspicuously altering the portions
of developmental stages and the sequence of
organ development from those observed
during indirect development (e.g. Fol, 1880;
Regondaud, 1964; Cumin, 1972: fresh water
basommatophorans; Meisenheimer, 1898;
Heyder, 1909; Ghose, 1963; Moor, 1977: stylommatophorans). In particular, the stylommatophorans thusfar investigated have several
transitory organs, such as a podocyst or
cephalic vesicle, that severely alter the shape
of developmental stages compared to the
primitive veliger type (for discussion see also
Fretter, 1975, p. xv-xvi). In particular, the slug-
360
B. RUTHENSTEINER
Figures 12-15, Onchidium c.f. branchiferum. Micrographs of sections of development stages. 12. Intermetamorphic stage, eight day post-settlement; transverse section. Scale bar = 50 (un. 13. 38 day postmetamorphic stage; sagittal section in the area of the kidney pore and anus. Scale bar = 50 u.m. 14. 37 day
post-metamorphic stage; transverse section. Arrow indicates the position of the genital duct developing from
the lung anlage epithelium. Scale bar = 50 (un. 15.37 day post-metamorphic stage (same specimen as Figure
14); transverse section through the kidney pore (arrow). Scale bar = 20 jj.m. Abbreviations: AN L, anlage of
the lung; CL, cloaca; F, foot; FO, foregut; G, ganglia; HG, hindgut; K, kidney; LD, pulmonary duct; ML,
midgut gland; PC, pallial cavity, PO, pallial cavity opening; RS, radula sac.
shaped species studied by Meisenheimer
(1898) and Heyder (1909) are not well suited
for interpreting development because the
important processes of shell and pallial formation are markedly suppressed during ontogeny.
Previous investigations of fresh water
basommatophoran and stylommatophoran
development reported two, more or less independent processes interpreted as (a) the
formation of the 'pallial cavity' and (b) the
invagination of the lung. However, the
development of the lung of Ovatella myosotis
reported here casts doubts on these interpretations. Two very similar processes are involved,
HOMOLOGY OF PALLIAL AND PULMONARY CAVITIES
361
Figure 16. Onchidium c.f. branchifcrum. etamorphic competent veliger. A. Lateral view. B. Dorsal view.
Abbreviations: F, foot; O, operculum; PC, pallial cavity; PR, pallial groove; V, velar lobes.
Figure 17. Onchidium c.f. branchiferum. Pallial complex of a two day post-metamorphic stage. A. Lateral
view. B. Dorsal view. Abbreviations: A, anus; HG, hindgut; K, kidney; KP, kidney pore; PC, pallial cavity.
which have to be interpreted in very different
ways. The misleading premise of all studies
that interpret the lung as secondarily derived is
their conception of the process of pallial cavity
formation in prosobranchs. This is typically
generalised by Raven (1966, p. 150): '. . . the
formation of the pallial cavity is due to the fact
that the mantle fold, in growing forwards along
the body, is elevated from the body wall, arching over the anal region . . .'. Accordingly, the
space that is usually first formed by forward
growth of the mantle in pulmonates has been
interpreted as 'pallial cavity.' It followed that
the deep invagination must be a newly
acquired structure. However, the pallial cavity
of prosobranchs is formed in a different way
than that stated by Raven (1966). In all the
prosobranch species investigated in this study
(Cellana sandwicensis, Gibbula adansonii,
Modulus tectum), the pallial cavity is formed
B. RUTHENSTEINER
362
CL
5 0 Mm
50 pm
Figure 18. Onchidium c.f. branchiferum. Pallial complex of a 19 day post-metamorphic stage. A. Lateral view.
B. Dorsal view. Abbreviations: A, anus; AN L, anlage of the lung; CL, cloaca; HG, hindgut; K, kidney, KP,
kidney pore.
Figure 19. Onchidium c.f. branchiferum. Diagrammatic sequence of the pallial complex development A. Two
day post-metamorphic stage. B. 12 day post-metamorphic stage. C. 26 day post-metamorphic stage. D. 37 day
post-metamorphic stage. E. 37 day post-metamorphic stage. F. 38 day post-metamorphic stage. G. 38 day postmetamorphic stage. H. Adult Abbreviations: HG, hindgut; K, kidney; blackstippling, pallia! cavity; dark-grey
stippling, lung; bright-grey stippling, cloaca; vertical striping, reproductive duct
primarily by invagination. This leads to two
conclusions: (1) Since pallial cavity formation
in Ovatella myosotis is the same as that in
these prosobranchs, the pallial cavity and the
lung of larva and adult Ovatella myosotis are
clearly homologous with the prosobranch pallial cavity. (2) Since pallial cavity formation in
prosobranchs (and O. myosotis) represents
mainly an invagination process, lung invagina-
tion in fresh water basommatophorans and
stylommatophorans may be regarded as a
homologous process. Thus the lung of these
pulmonates represents the pallial cavity.
Additional support for the general homology of the lung and pallial cavity in all major
gastropod taxa is supplied by the development
of opisthobranchs and of Amphibola crenata.
Pallial cavity formation in opisthobranchs
HOMOLOGY OF PALLIAL AND PULMONARY CAVITIES
363
20
Figures 20-21. Smeagol climoi. 20. Transverse section through the posterior end. Scale bar = 200 (im. 21.
Transverse section; detail of the pallial gland. Arrows indicate positions where gland cells open into the ducL
Scale bar = 50 pm. Abbreviations: HG, hindgut; K, kidney; L, left side; N, nuclei of gland cells; PC, pallial
cavity; PG, pallial gland; R, right side.
Figure 22. Smeagol climoi. Posterior end (same specimen as Figure 20-21). A. Lateral view. B. Dorsal view.
Abbreviations: HG, hindgut; K, kidney, KP, kidney pore; PC, pallial cavity; PG, pallial gland.
follows the same pattern shown for prosobranchs and O. myosotis (Smith, 1967: Retusa
obtusa; Schaefer, 1992: Haminaea navicula). In
Amphibola crenata, a member of the family
Amphibolidae that was classified among
pulmonates, the larval pallial cavity becomes
364
B. RUTHENSTEDMER
the 'lung' after metamorphosis (Little, Sterling, Pilkington & Pilkington, 1985). The pulmonate nature of the amphibolids has recently
come into question because of molecular data
(Tillier & Tillier, 1995; Tillier, Masselot &
Tillier, 1995) and nervous system characters
(Ruthensteiner, unpubl.). In summary, the
developmental features give no convincing
evidence for non-homology of the pulmonate
lung with the pallial cavity of the other gastropod groups.
Hontology of the onchidiid pallial complex
The systematic position of the family Onchidiidae has been a matter of debate for decades
(reviewed in Britton, 1984) because of pallial
complex characters. After their placement
among opisthobranchs and among a separate
grouping (gymnomorphs), they are now
regarded as true pulmonates by the majority of
authors (e.g. Tillier, 1984; Haszprunar &
Huber, 1990; Nordsiek, 1992; Tillier & Tillier,
1995). The reason for this family's separation
from the pulmonates has been the presence of
a lung opening separate from the pallial cavity.
Fretter's (1943) study of Onchidella celtica
deduced that the lung forms as a secondary
ectodermal invagination independent of the
pallial cavity. However, a closer examination
of Fretter's paper reveals that the report of
lung development is weakly supported by
data, due to the lack of respective developmental stages. Examination of the onchidiid
Onchidium c.f. branchiferum shows that the
lung actually is a part of the pallial cavity
because it develops from its most anterior portion, while the cloaca represents the remaining
pallial cavity. There is another major discrepancy between the Fretter's (1943) description
of the development of Onchidella celtica and
my observations on Onchidium c.f. branchiferum. Fretter possibly overlooked the deep
pallial cavity in the terminal larval stage, since
she described the pallial cavity as small and
lying on the right larval side, with the anus at
its innermost position.
At the first glance the formation of the
pallial complex of Onchidium c.f. branchiferum appears to differ fundamentally from
that of Ovatella myosotis. Only part of the pallial cavity becomes the lung; the size of the pallial cavity is reduced before the animal reaches
its slug-like shape; and the lung achieves a distinct secondary enlargement. These observations, however, do not contradict the concept
of a general homology of pulmonate lungs
because: (1) Comparison of lung formation of
O. myosotis with that of stylommatophorans
and fresh water basommatophorans shows that
differences in developmental processes may be
caused by factors such as yolk-richness during
development or overall body shape of the
adult. Such differences, therefore, do not
necessarily indicate the non-homology of the
onchidiid and ellobiid lung. The difference in
development seen in onchidiids may be highly
derived because of limacization (see Tillier,
1984) and complex metamorphosis. Hoffmann
(1929) and Tillier (1984) presented a plausible
model of the derivation of the onchidiid lung
from that of torted pulmonates. (2) The separation of a cloaca from the lung in onchidiids is
not unique among pulmonates as Plate (1891)
reported a cloaca with a separate opening from
the pneumostome in the stylommatophoran
genus Daudebardia (Zonitidae).
Another developmental feature that supports the homology of the pulmonate lung with
the pallial cavity of prosobranchs and opisthobranchs is that major components of the reproductive ducts are derived froin the lung
epithelium in Ovatella myosotis (herein),
Onchidium c.f. branchiferum (herein), and
Lymnaea stagnalis (see Fraser, 1946). This
occurs in a way similar to the formation of corresponding reproductive duct components
from the pallial cavity epithelium of prosobranchs (Guyomarc'h Cousin, 1976: Littorina
saxatilis) and opisthobranchs (Schaefer, 1992:
Haminaea navicula). The ontogenetic derivation of homologous elements of one organ system from another, supports the homology of
their precursor structures.
Adult morphology also provides substantial
evidence for the homologies proposed herein.
First, the location of the pallial cavity and lung
in prosobranchs, torted opisthobranchs and
pulmonates is identical. The pallial cavity and
lung share positional correlations with organs
such as the heart and kidney. In most pulmonates that have a simple excretory pore, this
pore lies within the lung distant from the
pneumostome. It should be noted here, that the
lung of many pulmonates may be filled with
water in life, it functions solely for air respiration only in some groups of pulmonates (see
Fretter, 1975). The pulmonate family Siphonariidae even has a gill within the lung for respiration when it is filled with water. The
homology of this gill with the prosobranch
ctenidium, however, is a matter of some debate
(e.g. Hubendick, 1947; Haszprunar, 1985).
When an osphradium is present, it lies within
365
HOMOLOGY OF PALLIAL AND PULMONARY CAVITIES
the lung some distance from the pneumostome. be regarded as a pallial cavity or as a lung. This
Although adult stylommatophorans do not structure lacks any morphological characterishave an osphradium, an embryonic osphradium
tic that clearly allows one to decide which of
has been reported in the lung anlage of Limax the two terms should be applied. It therefore
(Henchman, 1890) and Helix (Pelseneer, 1901). seems unjustified to use the formation of a lung
Pelseneer (1901) interpreted this as evidence as a synapomorphic character of pulmonates
for the homology of the stylommatophoran for a phylogenetic analysis. The opening of pullung (='cavit6 palliale') with that of the other monate pallial cavities/lungs (the so called
pulmonates. The (opposed) ciliary bands found pneumostome) shows distinct differences from
in water-filled pulmonate lungs were regarded the pallial cavity openings of prosobranchs: it
by Haszpninar (1985) as homologous to the is distinctly smaller and shifted to the right or
ciliary bands within the pallial cavities of lower posteriorly. One should, however, be cautious
heterobranchs and opisthobranchs.
when interpreting this as a synapomorphic
pulmonate character, because a similar
All authors studying the morphology of
primitive pulmonates such as siphonariids have organisation can be found in some primitive
regarded the lung as a clear homologue of the opisthonbranchs that have mantle cavities (e.g.
pallial cavity (Hubendick, 1947; Yonge, 1952; Fretter & Graham, 1954: Actaeon). The degree
Fretter, 1975). In his studies of Chilina, Brace to which the mantle cavity opening is narrowed
(1983) vigorously rejected the hypothesis of a may be equal in certain opisthobranchs
(Actaeon) and pulmonates (Hubendick, 1947:
secondary nature of the pulmonate lung.
Siphonaria). However, the literature contains
other characters of the nervous, digestive
The pallial gland ('lung') o/Smeagol
and reproductive systems that support the
The pallial complex of Smeagol can be re- monophyly of pulmonates (e.g. Haszprunar,
interpreted after detailed examination. As pre- 1985; Salvini-Plawen, 1991; Nordsiek, 1992).
viously suspected by Tillier & Ponder (1992)
Ontogeny of the pallial complex and lung in
the 'lung' is a gland. This voluminous organ, onchidiids is not fundamentally different from
which empties its glandular products into the that of other pulmonates, and therefore gives
pallial cavity has nothing to do with a lung. no clear support for a systematic placement of
Climo's (1980) interpretation of the organ as this group apart from pulmonates. Various
'lung' is surprising because his description characters of the nervous system (Van Mol,
lacks any indication that the organ contains 1967; Haszprunar & Huber, 1990), spermiospaces that are air filled in life. The 'lacunae' genesis (Tuzet, 1940; Healy, 1986) and the
of Climo's description appear to be the vac- genital system (Ghiselin, 1966; Ruthensteiner,
uoles of the gland cells.
1993), as well as molecular data (Tillier &
Tillier, 1995), strongly support the pulmonate
nature of the Onchidiidae and thus of the
Phylogenetic impact
Gymnomorpha (Systellomatophora).
There are two aspects that might give reason
The question of the homology of the pulto reconsider the systematic placement of
monate lung with the pallial cavity has been of
considerable significance for phylogenetic Smeagol. (1) This genus originally was placed
analyses. Certain pulmonate taxa, such as among pulmonates primarily because of its
stylommatophorans, have a typical, well- reported lung (Climo, 1980), which is now
characterized lung. The contractile pneumo- known to be a gland. Accordingly, the pallial
stome and typical blood lacunae arrangement cavity of Smeagol may now be considered
in the lung may be regarded as a synapo- homologous with the pulmonate lung. This
morphic organs. However, when looking at the cavity, however, does not resemble pulmonate
organisation of various pulmonate lungs there lungs in function or organisation. (2) Other
is no decisive characteristic that distinguishes characters must be examined to determine the
the pulmonate lung from the prosobranch systematic position of Smeagol because the
pallia! cavity. This can be demonstrated in presence of a lung can no longer be regarded
groups such as the glacidorbids or amphibolids as a synapomorphic character of pulmonates
whose systematic affinities to pulmonates are (see above). Haszprunar & Huber (1990)
currently under discussion (Ponder, 1986; emphasise the presence of certain cerebral
Haszpninar, 1988; Tillier & Tillier, 1995; ganglion characters, such as the procerebrum,
Tillier et al., 1995). Depending on the current as confirming a systematic position of Smeagol
classification, the same structure could either among pulmonates. Since the procerebrum is
B. RUTHENSTEINER
366
homologous with the opisthobranch rhinophoral ganglion (Ruthensteiner, unpublished),
this character also loses its diagnostic significance. Nordsiek (1992) suggested the presence
of single dorsal jaw as a synapomorphic feature of pulmonates, a structure that is absent in
Smeagol climoi (pers. obs.). One, therefore,
should not ignore the possibility of a closer
relationship of smeagolids to opisthobranchs
rather than pulmonates, as suggested by
Haszprunar (1985).
ACKNOWLEDGMENTS
I am indebted to L. Salvini-Plawen (Vienna) and
M.G. Hadfield (Honolulu) who provided laboratory
facilities. G. Haszprunar (Munich), S.A. Ridgway
(Munich), W.F. Ponder (Sydney) and an anonymous
referee provided valuable comments on the
manuscript M.G. Harasewych (Washington DC)
helped to improve the english. Thanks to W.F. Ponder for the material of Smeagol climoi. The study
was supported by grant J 0275 Bio of the Austrian
Science Foundation.
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