ANATOMY OF BATHYACMAEA SECUNDA OKUTANI, FUJIKURA & SASAKI, 1993 (PATELLOGASTROPODA: ACMAEIDAE)
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ANATOMY OF BATHYACMAEA SECUNDA OKUTANI, FUJIKURA
& SASAKI, 1993 (PATELLOGASTROPODA: ACMAEIDAE)
TAKENORI SASAKI 1 , TAKASHI OKUTANI 2 AND KATSUNORI FUJIKURA 2
1
The University Museum, The University of Tokyo, 7-3-1 Hongo, Bunkyo-ku, Tokyo, Japan 113-0033; and
2
Japan Agency for Marine-Earth Science & Technology, 2-15 Natsushima, Yokosuka, Kanagawa Prefecture, Japan 237-0061
(Received 3 September 2005; accepted 25 January 2006)
ABSTRACT
Anatomy of a vent-endemic patellogastropod limpet, Bathyacmaea secunda, was examined by gross dissection
and serial sections. It was revealed that B. secunda is anatomically distinct from other patellogastropod taxa
in that (1) the intestine runs through the ventricle; (2) the ventral approximator muscle of odontophoral
cartilages is ventrally single-layered; (3) there is a pair of radular teeth with long shafts; and (4) the sta-
tocysts are isolated from pleural and pedal ganglia. In addition, the species is characterized by short
pallial margin papillae, lack of pallial streaks, presence of a ctenidium, obliquely tubular salivary
glands, simple gut configuration and acmaeoidean type of buccal mass musculature and odontophoral
cartilages. The comparison in anatomical and shell microstructural characters suggests that B. secunda
shares no unique similarities with the Patelloidea or Neolepetopsidae and, therefore, is not closely
related to these groups. In contrast, a number of similarities were found between B. secunda and
acmaeid species. These results support the current systematic position of Bathyacmaea within the Acmaei-
dae, although anatomical data from some related genera are still insufficient.
INTRODUCTION North Knoll of Iheya Ridge, Okinawa Trough (1049 m deep,
Shinkai 2000 Dive 863; 1390 m deep, Shinkai 2000 Dive 672) (see
At higher taxonomic levels, patellogastropods exhibit more strik- Sasaki et al., 2003: table 1 for details; Sasaki et al., 2005, for
ing complexity in anatomy and shell microstructure than in map). The specimens were fixed in 10% formalin and preserved
gross shell morphology (Lindberg, 1988, 1998; Sasaki, 1998; in 70% ethanol. The gross morphology was observed under a
Fuchigami & Sasaki, 2005). Therefore, comparative anatomy binocular microscope. The animals of eight specimens from the
of soft parts is important in systematic and phylogenetic Minami-Ensei Knoll were embedded in paraffin, sectioned at
studies. Nevertheless, a large number of patellogastropods, 6 – 8 mm and stained with haematoxylin and eosin. Whole sets
especially those from deep-sea environments, have been insuffi- of histological sections are registered and deposited in the
ciently investigated to date. Department of Historical Geology, The University Museum,
Bathyacmaea is one of the poorly investigated groups of the The University of Tokyo (registration numbers UMUT
Patellogastropoda. The genus is endemic to deep-sea RM29012– RM29019). The terminology of descriptions in this
chemosynthesis-based communities in vents or seeps (Warén & study follows Sasaki (1988).
Bouchet, 2001: appendix 2; Sasaki et al., 2003). It has been
assigned to the Acmaeidae (Pectinodontinae) for three reasons:
(1) the presence of foliated shell structure; (2) the presence of RESULTS
the ctenidium; and (3) a single pair of tricuspid radular teeth
whose components might be comparable to those of Pectinodonta
External anatomy
(Okutani et al., 1993). No other anatomical characters, however, The animal is longitudinally oval, dorsoventrally depressed and
have been observed and little has been discussed concerning the bilaterally symmetrical in outline (Figs 1 – 3). The dorsal surface
higher systematic position of the genus. Furthermore, it is inter- is covered with a thin epithelium. The animal in dorsal view is
esting to compare Bathyacmaea with another group of vent- divisible into the mantle margin, the attachment area of the
endemic limpets, the Neolepetopsidae (Fretter, 1990; McLean, shell muscle, the pallial cavity and the visceral mass.
1990; Warén & Bouchet, 2001). The mantle is fringed with minute pallial margin papillae
To clarify the anatomical organization of Bathyacmaea, we (Figs 1, 2: cpt), which are entirely retractile into the mantle margin
observed the soft parts of B. secunda by gross dissection and and invisible in most specimens. However, their presence is clear in
serial sections. Unfortunately, the type species (B. nipponica ) histological sections, where the epithelium of the papillae can be
has not been collected since its original description (Okutani seen as circlets in horizontal sections (Fig. 4C). A periostracal
et al., 1992). Using new data revealed in this study, the body groove was not clear in cross sections. A sensory stripe with neuro-
plan of Bathyacmaea is compared with that of other patellogastro- lymphoid tissue on the inner mantle wall (as found in lepetids;
pods and its implications for higher systematics are discussed. Angerer & Haszprunar, 1996) is absent.
The attachment area of the shell muscle to the shell is
horseshoe-shaped, surrounding the visceral mass and nearly
MATERIAL AND METHODS divided into 11 bundles (Fig. 1). The mantle over the head is
suspended by a thin pallial muscle whose attachment area is
Material used in this study was collected from the Minami-Ensei continuous with both anterior ends of the shell muscle.
Knoll, Okinawa Trough (700 m deep, Shinkai 2000 Dive 547) On the dorsal surface, the visceral mass consists of the diges-
(see Okutani et al., 1993: table 1 for details) and from the tive gland in the centre, the final loop of the intestine, the
dorsal part of the gonad (in ripe condition), the pericardium
Correspondence: T. Sasaki; e-mail: sasaki@um.u-tokyo.ac.jp and the right kidney (Fig. 1). On the ventral side (Fig. 2), the
Journal of Molluscan Studies (2006) 72: 295– 309. Advance Access Publication: 26 May 2006 doi:10.1093/mollus/eyl007
# The Author 2006. Published by Oxford University Press on behalf of The Malacological Society of London, all rights reserved.T. SASAKI ET AL.
foot is smoothly continuous with the shell muscle. Neither epipo-
dial folds nor tentacles are developed on the surface. Pallial
streaks (cf. Sasaki, 1998: Figs 1b, 4b) are absent along the pedal
wall and shell muscle. The pedal sole and lateral wall are clearly
distinguishable in histological preparations. The former is
covered with tall epithelial cells (Fig. 4A: pse), whereas the epi-
thelium of the latter is very thin (Fig. 4B). The anterior pedal
glands (Fig. 4B: apg) are concentrated along the anterior margin
of the pedal sole. The lateral pedal glands (Fig. 4B: lpg) are sparse
and scattered subepithelially along the lateral pedal wall.
The head is situated in front of the foot, is shorter than wide
and composed of the snout and a pair of cephalic tentacles.
The snout is short, stout and bends ventrally. The mouth
opens in the centre and is surrounded by the thickened and
reflected fringe of the outer lip (Fig. 2: ol). A pair of inner lips
(Fig. 2: il) originates from the lateral wall of the oral tube and
only their central part is visible when the mouth is open
(Fig. 2). Oral lappets are absent.
The cephalic tentacles arise from the sides of the head and are
variably contracted in fixed specimens. The surface of the tenta-
cles is smooth under gross examination. No trace of eyes is found,
even in histological sections around the bases of the cephalic
tentacles.
The pallial groove encircles the pedal sole and connects with
Figure 1. Dorsal view of animal, with part of mantle removed to show the pallial cavity (nuchal cavity) above the head. No secondary
pallial cavity and heart. Abbreviations: a, anus; cl, ctenidial lamella; respiratory structure is developed along the circumpallial sinus
ct, cephalic tentacle; dg, digestive gland; ecs, efferent ctenidial sinus; in the pallial groove.
eps, efferent pallial sinus; I, intestine; lk, left kidney; lko, left kidney
opening; mm, mantle margin; ov, ovary; pc, pericardium; pmp, pallial
margin papilla; rk, right kidney; rko, right kidney opening; sm, shell
muscle; sn, snout; st, stomach; v, ventricle. Pallial cavity
The pallial cavity is deep for patellogastropods and attains
pedal sole, the head, the pallial groove (Fig. 2: pg) and the approximately 50% of the body length (Fig. 1). The inside of
mantle margin can be seen. the pallial cavity contains the ctenidium (Fig. 1), the openings
The pedal sole is oval in outline and elongate longitudinally of the right and left kidneys (Fig. 1: rko, lko) and the anus
(Fig. 2). The propodium (Fig. 3: pp) is weakly developed and (Fig. 1: a). Osphradia and hypobranchial glands are lacking.
located between the pedal sole and snout. The lateral wall of the The ctenidium is well developed, arises from the left posterior
wall of the pallial cavity and extends obliquely towards the
anterior right. It is composed of the ctenidial lamellae, the affer-
ent ctenidial sinus on the right side and the efferent ctenidial
sinus on the left side. In cross section, the lamellae are arranged
alternately (Fig. 4D) on dorsal and ventral sides. The surface of
the ctenidial lamellae is ciliated but lacks distinctly organized
ciliary bands. There are no skeletal rods or sensory pockets
within the lamellae.
Digestive system
The digestive system consists chiefly of (1) the pre-oesophageal
digestive tract including mouth, oral tube, sublingual cavity
and buccal cavity; (2) the jaw; (3) the buccal mass including
radula and odontophoral cartilages; (4) the salivary glands;
(5) the radular sac; (6) the oesophagus; (7) the stomach with
digestive glands; and (8) the intestine and anus (Fig. 5).
The oral tube is represented by a short space between the
mouth and the inner lips and is followed ventrally by the sublin-
gual pouch (Figs 6D, 7: slp) and dorsally by the buccal cavity.
The sublingual pouch is a dorsoventrally depressed sac below
the anterior part of the buccal mass. Its epithelium is composed
of a single layer of tall columnar cells with basal nuclei and it is
surrounded by glandular tissue (Fig. 6D). The dorsal wall of the
buccal cavity is thickened with a pair of dorsal folds defining the
dorsal food channel (Fig. 5: dfc). The surface lateral to the dorsal
folds is thickened with tall glandular cells.
Figure 2. Ventral view of animal. Abbreviations: ct, cephalic tentacle; il, The anterodorsal wall of the buccal cavity is reinforced by the
inner lip; mm, mantle margin; ol, outer lip; pcv, pallial cavity; pg, pallial jaw. The jaw is single, not divided into a pair and consists of
groove; pmp, pallial margin papilla; ps, pedal sole; sm, shell muscle; sn, the anterior wings, posterior wing and anterior band
snout. (Fig. 8A). The anterior margin of the jaw is double-layered,
296ANATOMY OF BATHYACMAEA
Figure 3. Longitudinal section of animal (UMUT RM29018). Abbreviations: ac, anterior cartilage of odontophore; acs, afferent ctenidial sinus; aw,
anterior wing of jaw; bcv, buccal cavity; cl, ctenidial lamella; dg, digestive gland; i, intestine; lk, left kidney; m, mantle; me, mid-oesophagus; mm,
mantle margin; mo, mouth; ol, outer lip; ov, ovary; pcd, pedal nerve cord; pp, propodium; ps, pedal sole; pw, posterior wing of jaw; rd, radula; rk,
right kidney; sm, shell muscle; st, stomach; ts, typhlosole.
with overlap between the anterior band and posterior wing. The The buccal mass consists of the licker, odontophoral carti-
anterior wings are attached to the inner lips and the inner layer lages, radula and their associated musculature. The licker
of the lateral protractor muscles (Fig. 7: lp). The posterior wing (Fig. 6B: lic) is located at the anterior tip of the subradular mem-
is joined by anterolateral cartilages to muscular attachments. brane, in front of the first row of radular teeth. Its surface is
Figure 4. Histological sections of foot, mantle and ctenidium. A. Cross section of mid-ventral part of foot. B. Cross-section of marginal part of foot;
arrowhead indicates boundary between pedal sole (left) and outer lateral wall of foot (right). C. Horizontal section of mantle. D. Vertical section
of ctenidium. A, D. UMUT RM29018. B. UMUT RM29012. C. UMUT RM29017. Abbreviations: apg, glandular cell in anterior part of foot;
ca, ctenidial axis; cl, ctenidial lamella; clm, cuticularized layer of mantle; lpg, glandular cell in lateral part of foot; mm, mantle margin; pcv,
pallial cavity; pm, pedal muscle; pse, epithelium of pedal sole; psn, pedal sinus.
297T. SASAKI ET AL.
The buccal cavity is inflated laterally above the odontophore
and followed by the oesophagus. The frontal floor of the oeso-
phagus is marked by a flap-like oesophageal valve (Fig. 9: ev).
There is a large, flat space between the oesophageal valve and
subradular membrane (srm), termed the radular diverticulum
(Fig. 9: rdv). The oesophagus is divided into three sections
(anterior, mid and posterior) by differences in width, cross-
section and inner structure. The anterior oesophagus contains
the dorsal food channel, dorsal folds, ventral folds and lateral
oesophageal pouches (Fig. 11A –C). Two longitudinal, dorsal
folds delimit the dorsal foot channel (dfc). The ventral folds lie
outside the dorsal folds in the anterior part (Fig. 11A), but are
shifted inwards posteriorly (Fig. 11B, C). The lateral walls are
swollen to form the lateral pouches (lep), which are striated by
transverse interior folds (Fig. 5). The inner walls of the oesopha-
geal pouches are glandular (Fig. 11C). The mid-oesophagus
(Fig. 5: me) is defined by the decrease in width, absence of
oesophageal pouches and the 1808 rotation as a consequence of
torsion. Its inner wall shows numerous transverse infoldings
of the glandular epithelium. The dorsal and ventral folds are
close together (Fig. 11D); the ventral folds are fused at their
bases, whereas dorsal folds remain unfused (Fig. 11D). The pos-
terior oesophagus (Fig. 5: pe) is a simple tube, the narrowest part
of the oesophagus and is corrugated inside by longitudinal ridges
and grooves (Fig. 11E).
The stomach (Fig. 5: st) is C-shaped and defined by the increase
Figure 5. Configuration of digestive tract, salivary glands and radular
in the diameter of the digestive tract following the posterior
sac. Abbreviations: a, anus; bcv, buccal cavity; dfc, dorsal food oesophagus. Only a small part is visible on the dorsal surface
channel; dgo, digestive gland opening; i, intestine; lep, lateral pouch of (Fig. 1), because most of the stomach is covered by the digestive
anterior oesophagus; me, mid-oesophagus; pe, posterior oesophagus; glands. The interior surface is longitudinally striated anteriorly
rds, radular sac; sg, salivary gland; st1, striated region of stomach; st2, (Fig. 5: stl), but the rest is smooth (Fig. 5: st2), except for a
smooth region of stomach. shallow intestinal groove marked by a pair of obsolete typhlosoles
(Fig. 3: ts). Neither gastric shield nor caecum is present.
The digestive glands cover both dorsal and ventral sides of the
macroscopically smooth; in cross section there is a single layer of stomach. The dorsal lobe extends broadly over the visceral mass
cells, thickened medially. The buccal mass contains two pairs of on the dorsal surface. The ventral lobe is situated between the
odontophoral cartilages (Fig. 8B, C). The anterior cartilages stomach and the gonad. Both lobes are connected to the initial
(ac) support the odontophore along their entire length. The part of the stomach behind the posterior oesophagus (Fig. 5).
anterolateral cartilages (alc) are attached to the dorsolateral The intestine (Fig. 5: i), recognizable as a narrower part of the
anterior corner of the anterior cartilages. Their posterior tract distal to the stomach, makes four loops. Their detailed con-
sides are roundly swollen and their anterior sides are sharply figuration is slightly variable, but the four-loop pattern is con-
pointed. sistent; the final loop runs through the ventricle (Fig. 11F). In
The radula consists of the radular teeth, the basal plates, the cross section, the intestine is nearly circular along most of its
radular membrane and the subradular membrane (Figs 6E – F, length, although the terminal part is heavily corrugated and dis-
10). Anterior rows of the radular teeth are exposed in the tinguishable as the rectum. The anus opens at the right posterior
buccal cavity anterior to the oesophageal valve. The radular corner of the pallial cavity (Fig. 1).
formula is 0 – 1 – 0 –1 – 0. The tip of each lateral tooth is dark
brown, mineralized and divided into three cusps (Fig. 10: cs1 –
3); the shaft (s) is opaque; the basal plate (bp) stains deep red Buccal musculature
in histological sections (Fig. 6E, F). Over the buccal mass, the
The muscles of the buccal mass (Figs 7, 9) are positionally and
radular membrane is extended laterally to form the subradular
functionally categorized into three groups: (1) muscles controlling
membrane (Fig. 6E: srm). Posterior to the buccal cavity, the
the odontophore; (2) muscles attached to the subradular mem-
radula is enclosed within radular sac (Fig. 5: rds). The radular
brane; and (3) muscles connecting the odontophoral cartilages.
sac is separated from the posterior part of the buccal mass and
embedded in the visceral mass (Fig. 5). It is not very long for
patellogastropods, forming a single loop behind the odonto- (1) Muscles controlling the odontophore. The odontophore is
phore, just to the right of the visceral mass. The free portion of fixed to the body wall by dorsal, lateral and ventral protrac-
the radular sac is mostly below the digestive tract except for tor muscles and by anterior levator muscles. The dorsal pro-
the posterior folded part. The end of radular sac is expanded tractor muscles are thin, weakly developed and
as a simple, club-shaped mass. membranous, connecting the posterior part of the buccal
The salivary glands (Figs 5, 11A: sg) are not massive but mass to the anterodorsal part of the head. The lateral pro-
tubular and situated along the outer margin of the lateral oeso- tractor muscles (lp) originate from the anterolateral wall
phageal pouches (lep) over the buccal mass. The salivary ducts of the snout and insert on the posterior end of the anterior
run along the inside of the glands and the ducts proper are cartilage. The ventral protractor muscles (vp) consist of
limited to the short anterior portion. They are separated from two layers. The outer ventral protractor muscles (ovp) orig-
the lateral oesophageal pouches and open into the buccal cavity inate from the body wall behind the mouth and pass ven-
at its posterolateral sides. Both right and left glands are anterior trally under the remaining buccal musculature. The inner
to the circumoesophageal nerve ring and do not pass through it. ventral protractor muscles (ivp) arise from the outer
298ANATOMY OF BATHYACMAEA
Figure 6. Histology of organs in buccal region. A. Longitudinal section of anterior part of jaw. B. Cross section of licker (lic) and adjacent structures. C.
Vertical section of anterior odontophoral cartilages. D. Cross-section of sublingual pouch (slp) and connective structures between anterior odonto-
phoral cartilages (aca). E. Cross section of radula above buccal mass. F. Longitudinal section of radula enclosed in radular sac. A. UMUT
RM29018. B, E. UMUT RM29016. C, D. UMUT RM29013. F. UMUT RM29014. Abbreviations: ab, anterior band of jaw; ac, anterior cartilage
of odontophore; bcv, buccal cavity; bp, basal plate of radula; bs, buccal sinus; cs, cusp of radular teeth; ict, inter-cartilage connective tissue; il, inner lip;
mpr, median protractor muscle of subradular membrane; pw, posterior wing of jaw; rm, radular membrane; s, shaft of radular teeth; slp, sublingual
pouch; srm, subradular membrane; vap, ventral approximator muscle of odontophoral cartilages.
surface of the sublingual pouch (slp). Both layers insert on the subradular membrane. They consist of the retractor
the posterior end of the anterior cartilages on the ventral muscles of the subradular membrane (rsr), the median pro-
side. The anterior levator muscles (al) originate from the tractor muscles of the subradular membrane (mpr) and the
body wall of the head and inset on the anterolateral lateral protractors of the subradular membrane (lpr). The
corner of the odontophore, along the anterolateral cartilages retractor muscles (rsr) are attached to the main area of
and the margin of the posterior wing of the jaw. the subradular membrane and the ventrolateral side of the
(2) Muscles attached to the subradular membrane. The muscles anterior cartilages. They occupy the largest volume
related to radular movement attach to the ventral surface of among the muscles in the buccal mass. The right and left
299T. SASAKI ET AL.
Figure 7. Ventral view of buccal mass; lateral protractor muscle and Figure 9. Dorsal view of buccal mass, with dorsal protractor muscles of
outer ventral protractor muscle of odontophore have been removed on odontophore removed. Abbreviations: ab, anterior band of jaw; al, ante-
left side. Abbreviations: ab, anterior band of jaw; aw, anterior wing of rolateral levator muscle; alc, anterolateral cartilage of odontophore; bg,
jaw; il, inner lip; ivp, inner ventral protractor muscle of odontophore; buccal ganglion; cc, cerebral commissure; drd, dilator muscle of radular
lp, lateral protractor muscle of odontophore; lpr, lateral protractor diverticulum; ev, oesophageal valve; lp, lateral protractor muscle of
muscle of subradular membrane; mpr, median protractor muscle of sub- odontophore; pw, posterior wing of jaw; rds, radular sac; rdt, radular
radular membrane; ovp, outer ventral protractor muscle of odonto- teeth; rdv, radular diverticulum; rev, retractor muscle of oesophageal
phore; rds, radular sac; rsr, retractor muscle of subradular membrane; valve; rrd, retractor muscle of radular diverticulum; rsr, retractor
slp, sublingual pouch; tlm, transverse labial muscle; vap, ventral approx- muscle of subradular membrane; srm, subradular membrane.
imator muscle of odontophoral cartilages.
Figure 8. Jaw and odontophoral cartilages. A. Dorsal view of jaw. B. Figure 10. Scanning electron micrograph of radula (UMUT
Dorsal view of odontophoral cartilages. C. Ventral view of odontophoral RM29199). Abbreviations: sc1–3, cusp1–3; rbp, median ridge of basal
cartilages. Abbreviations: ab, anterior band of jaw; ac, anterior cartilage plate.
of odontophore; alc, anterolateral cartilage of odontophore; aw, anterior
wing of jaw; ict, inter-cartilage connective tissue; pw, posterior wing of
jaw; vap, ventral approximator muscle of odontophoral cartilages. line of the buccal mass, between the sublingual pouch and
the ventral approximator muscle of the odontophoral carti-
muscles are clearly separated into a pair and not fused into a lages (vap). The lateral protractor muscles (lpr) originate
single layer. The median protractor muscles (mpr) originate from the posterior end of the anterior cartilage and insert
from the body wall below the posterior part of the buccal on the subradular membrane posterior to the licker. They
mass and insert beneath the licker. They are thin and fila- are more than twice as thick as the median protractor
mentous, but distinct from other muscles. The right and muscles of the radula (mpr). Each of these paired muscles
left muscles are close to each other and run along the sagittal lies lateral to the median protractor muscles of the radula
300ANATOMY OF BATHYACMAEA
Figure 11. Histology of digestive tract and associated structures. A. Cross section of anterior part of anterior oesophagus. B. Cross section of anterior
oesophagus slightly posterior to A. C. Cross section of anterior oesophagus at level of posterior end of buccal mass. D. Cross section of middle part of
mid-oesophagus. E. Cross section of posterior oesophagus (pe). F. Longitudinal section of intestine (i) running through both pericardium (pc) and
ventricle (v). A, B. UMUT RM29016. C. UMUT RM29012. D. UMUT RM29017. E, F. UMUT RM29014. Abbreviations: ac, anterior cartilage
of odontophore; df, dorsal folds of oesophagus; dfc, dorsal food channel; i, intestine; lep, lateral pouch of anterior oesophagus; ov, ovary; pc, pericar-
dium; pe, posterior oesophagus; rds, radular sac; rdt, radular teeth; rsr, retractor muscle of subradular membrane; sg, salivary gland; t, testis; v, ven-
tricle; vf, ventral folds of oesophagus.
(mpr) and ventral protractor muscles of the odontophore This connective tissue is somewhat cartilage-like, but its ves-
(ovp, ivp). icular units are much smaller and denser than those of the
(3) Muscles connecting the odontophoral cartilages. The ventral anterior and anterolateral cartilages (Fig. 6C).
side of the anterior cartilages (aca) are united by the ventral
approximator muscle (vap) for the anterior two-thirds of
their length (Fig. 6C). The cartilages are also connected by
another sheet-like structure at a more dorsal level. Histologi-
Excretory organ
cally, this is not muscular but is a connective tissue, termed The excretory organ consists of the pericardial cavity, left reno-
here the ‘intercartilage connective tissue’ (Figs 6D, 7B: ict). pericardial duct and left and right kidneys. The kidneys are
301T. SASAKI ET AL.
greatly asymmetrical and both of them are separate from the than the auricle and is triangular in outline. Its muscle fibers
pericardium on the right side and on either side of the intestine. are clearly seen in gross dissection. Most of the ventricle is free
The pericardium (Fig. 1: pc) is situated at the left anterior within the pericardium except at three attachment points, one
corner of the visceral mass, attached to the shell muscle; it is at the connection with the auricle and two at the right and pos-
triangular in outline and encloses the heart. The presence of terior corners of the pericardium.
podocytes within the pericardium was not confirmed in this The bulbous aorta is obliquely elongate, almost concealed
study. Its lumen is connected to the left kidney through the reno- below the ventricle and connected to the ventricle through a
pericardial duct that lies between the right anterior corner of the long slit. The inner wall of the bulbous aorta is muscular, like
pericardium and the left kidney. that of the ventricle. The ends of the bulbous aorta join the
The left kidney (Fig. 1: lk) is much smaller than the right, anterior and posterior aorta. The posterior aorta is short and
situated within the anteriormost part of the visceral mass that opens into the visceral sinus, associated with the gonad, digestive
bulges into the pallial cavity. Its epithelium is thin and gland and kidneys. The anterior aorta passes below the floor of
simple (Fig. 12A). The opening of the left kidney (lko) is trans- the pallial cavity and opens into the buccal sinus within the
versely slit-like (Fig. 1). The right kidney (Fig. 1: rk) surrounds buccal mass.
the digestive glands and the stomach, alongside the shell A small sinus abutting the left kidney has a connection to the
muscle, except in the pericardial region. The opening of the afferent ctenidial sinus and eventually to the efferent ctenidial
right kidney (rko) extends as a long tube and ends as a longi- sinus (Fig. 1: ecs). The ctenidial lamellae contain blood spaces
tudinal slit (Fig. 1). The inside of this tube is heavily ciliated (Fig. 4D). The fine sinuses from the visceral sinus pass through
(Fig. 12B). the shell muscle towards the circumpallial sinus in the mantle
margin.
Circulatory system
Reproductive system
The heart is enclosed within the pericardial cavity and is com-
posed of a single (left) auricle, the ventricle, and the aortic The animal is gonochoristic. The reproductive organs consist
bulb. The auricle (Fig. 1: au) is attached to the ctenidial base only of the gonad and a simple gonoduct; there is no copulatory
and connected to the efferent pallial sinus (eps), the pallial organ in the male.
sinus over the pallial cavity and the efferent ctenidial sinus The gonad lies ventral to the digestive tract and glands. The
(ecs) through several pores. Its wall is not muscular but thin. sexes are distinguishable in appearance when the gonad is ripe.
The ventricle (Fig. 1: ve) is much larger and more muscular The ovary contains eggs 150 mm in diameter (Fig. 12C) and
Figure 12. Histology of excretory and reproductive organs. A. Longitudinal section of excretory opening of right kidney (rko). B. Longitudinal section
of left kidney (lk) located in front of rectum (r). C. Ovary containing growing ova. D. Testis partitioned into vertical units. A, B. UMUT RM29018. C.
UMUT RM29017. D. UMUT 29012. Abbreviations: cl, ctenidial lamella; lk, left kidney; m, mantle; pcv, pallial cavity; r, rectum; rko, right kidney
opening; st, stomach; vs, visceral sinus.
302ANATOMY OF BATHYACMAEA
appears granular in external view. The testis is an aggregation of (apn, ppn). The pedal ganglia give off a pair of thick pedal cords
elongate units that contain radially arranged spermatozoa posteriorly.
(Fig. 12D). From the outside, the testis does not seem granular. Two subsidiary ganglia, the labial and buccal ganglia, are
In both sexes, as it grows, the gonad appears on the dorsal formed around the circumoesophageal nerve ring (Fig. 13).
surface on the left side of the visceral mass. In the most mature The labial ganglia (lg) are located on the ventral side of the
specimen, the anterior part of the gonad extends to the head oral tube connected with the cerebral ganglia by narrow connec-
region. tives and send thin nerves to the labial region. The buccal
The gonoduct extends from the left dorsal side of the gonad to ganglia (bg) lie above the radular diverticula along the posterior
the left anterior corner of the right kidney. There is no glandular margin of the buccal cavity. They supply nerves to the buccal
section of the gonoduct and no direct connection between the cavity, anterior oesophagus and various muscles associated
pericardium and the gonoduct. The right kidney opening also with the buccal mass. These ganglia are connected with each
functions as a reproductive opening. other by a commissure above the radular sac (Fig. 9) and with
the posterior side of the labial ganglia through connectives
extending along the lateral wall of the odontophore.
Nervous system The visceral loop is formed of the supra- and sub-oesophageal
parts of the pleurovisceral connectives (spv, sbv) and visceral
The nervous system is composed mainly of (1) the circumoeso- ganglion (vg) (Fig. 13). The supraoesophageal part is shorter
phageal nerve ring in the head region; (2) the visceral loop and lies more dorsally than the suboesophageal part. Separate
mainly in the anterior part of the visceral mass; and (3) the supraoesophageal and suboesophageal ganglia are not formed
pedal cords embedded in the pedal musculature (Fig. 13). in the visceral loop. The visceral ganglion is located below the
The circumoesophageal nerve ring is of the hypoathroid type left kidney and sends nerves to the kidneys and digestive organs.
and consists of three major pairs of ganglia, the cerebral, pleural Histologically the ganglion is cord-like and identified by swellings
and pedal ganglia. The cerebral ganglia (Fig. 13: cg) are located and emitted nerves. A nerve from the left side of the visceral
at the bases of the cephalic tentacles connected to the cerebral ganglion extends into the pericardium along the ctenidial base.
commissure (cc) in front of the posterior wing of the jaw and The pedal cords (Fig. 13: pcd) are embedded entirely within
send nerves to the cephalic tentacles and labial region of the the pedal musculature and many thin nerves extend from them
snout. The pleural (plg) and pedal ganglia (pdg) are adjacent ventrolaterally (Fig. 14A, B). They are connected posteriorly in
and situated below the posterior end of the buccal mass a circular form by a commissure.
(Fig. 13). They are linked with the cerebral ganglia by way of
cerebropleural and cerebropedal connectives (cdc, cpc), respect-
ively. The pedal ganglia are situated more posteromedially than Sense organs
the pleural ganglia. The pleural ganglia give rise to the visceral
loop and the pallial nerves. Each pallial nerve is a single branch The organs presumed to have sensory function include the
at the base but divides into anterior and posterior pallial nerves pallial margin papillae, the cephalic tentacles (see External
Anatomy), the licker (see Digestive System) and the statocysts.
Neither eyes nor osphradium (wart organ) are present. A pair
of statocysts is located on the posterolateral sides of the pleural
ganglia above the pedal musculature, far from the pedal
ganglia (Fig. 13: sta). They are markedly depressed dorsoven-
trally and contain numerous statoconia (Fig. 14C, D).
DISCUSSION
It is widely acknowledged that internal anatomy is more infor-
mative than gross shell morphology in recognizing higher taxo-
nomic categories of patellogastropods. As outlined by Lindberg
(1988, 1998) and Sasaki (1998), various suprageneric taxa have
been defined on the basis of shell microstructure and anatomical
characters. In the following discussion, we focus on the simi-
larities and dissimilarities between Bathyacmaea and other patel-
logastropods in anatomical characters. The systematic
implications of shell microstructural characters, including new
data on B. secunda, have been discussed in detail elsewhere
(Fuchigami & Sasaki, 2005). The results of the comparison of
anatomical characters are summarized in Tables 1 and 2, as a
basis for the higher systematics of patellogastropods.
Comparative anatomy
The possession of retractile pallial margin papillae is one of the
distinctive characteristics of patellogastropods. The papillae are
Figure 13. Nervous system and statocysts. Abbreviations: apn, anterior divided into two types, long in the Patellidae and Nacellidae
pallial nerve; bg, buccal ganglion; cc, cerebral commissure; cdc, cerebro-
(e.g. Sasaki, 1998: figs 4b, 10a) and short in the Neolepetopsidae,
pedal connective; cg, cerebral ganglion; cpc, cerebropleural connective;
lc, labial commissure; lg, labial ganglion; np, nerve to pericardium; nsn, Acmaeidae, Lepetidae and Lottiidae (e.g. Fretter, 1990;
nerve to snout; pcd, pedal nerve cord; pdg, pedal ganglion; plg, pleural Angerer & Haszprunar, 1996; Sasaki, 1998). Papillae of the
ganglion; ppn, posterior pallial nerve; sbv, suboesophageal part of visc- latter type, as found in B. secunda, can be completely retracted
eral loop; spv, supraoesophageal part of visceral loop; sta, statocyst; tn, into the inner fold of the mantle margin and appear to be
tentacular nerve; vg, visceral ganglion. absent when retracted. In B. secunda, the presence of the papillae
303T. SASAKI ET AL.
Figure 14. Histology of nervous system and sense organs. A. Cross section of the pair of pedal cords (pcd) running in pedal musculature (pm). B. Longi-
tudinal section of pedal cord (pcd). Asterisks indicate peripheral nerves extending into pedal musculature. The left side of the figure is the anterior of the
animal. C. Cross section of statocyst (sta). D. Magnified view of statocyst showing statoconia (stc). A. UMUT RM29012. B, D. UMUT RM29018. C.
UMUT RM29016. Abbreviations: ov, ovary; pcd, pedal nerve cord; plg, pleural ganglion; pm, pedal muscle; sta, statocyst; stc, statoconium; t, testis;
vs, visceral sinus.
is confirmed in histological sections (Fig. 4C), although the inner structure (Haszprunar, 1998: 380; Ponder & Lindberg,
majority of observed specimens seemed devoid of them externally. 1997: 109; Sasaki, 1998: 172, 175).
The mouth is surrounded by oral lappets in some patellogas- The jaw of Bathyacmaea is of typical patellogastropod type,
tropods (Neolepetopsidae, Lepetidae, Acmaeidae), but lacks with anterior and posterior wings attached to the inner lip and
such a specialized structure in the remaining groups including odontophore. The detailed morphology does not exhibit any
Bathyacmaea. It is unclear whether this character is useful in significant differences throughout the patellogastropods and is
higher systematics or not. Functionally, the lappets may serve of little systematic value.
to hold food item while grazing. There seems to be no clear cor- In its odontophoral cartilages, Bathyacmaea belongs to the two-
relation between their presence and habitat. pair type, as found in the Acmaeidae, Lottiidae and Lepetidae,
The lateral wall of the shell muscle is smooth in B. secunda, as in rather than to the three- to five-pair types of the Patelloidea. In
most patellogastropods except the Patelloidea (Patellidae and basal gastropods, vetigastropods and Cocculinida, there are also
Nacellidae). Most members of the Patelloidea have ridged struc- two pairs of cartilages, but these consist of anterior and posterior
tures termed ‘anterior and lateral pallial streaks’ (Sasaki, 1998) pairs unlike the anterior and anterolateral cartilages in the
or ‘lateral glandular grooves’ (Fretter & Graham, 1994: Acmaeoidea (Sasaki, 1998). Therefore, this character state diag-
fig. 339; Ridgway et al., 1998). We confirmed that such a struc- noses the Acmaeoidea (sensu lato ) in current systematics. The
ture is absent, even in a very immature specimen, in B. secunda. state in the Neolepetopsidae should be reexamined for clear
In the Patellidae, the lateral glandular groove is lost with growth comparison.
in most species, but is retained in some (Ridgway et al., 1998). The labial cartilages described by Sasaki (1998) in Cellana
The respiratory system of patellogastropods can be classified toreuma were not found in Bathyacmaea and are possibly autapo-
into four types: (1) ctenidium only; (2) secondary gills only; morphic for the genus Cellana.
(3) both ctenidium and secondary gills present; and (4) no gill The licker (also termed the subradular organ) at the anterior
(see Lindberg, 1988 for details). That of Bathyacmaea is of the tip of the subradular membrane is smooth in the Acmaeidae
first type, and this state is also found in Acmaeidae and Lottiidae including Bathyacmaea, Lottiidae and Lepetidae, but sharply
(except Erginus: Lindberg, 1988; Sasaki, 1998). Possession of a lamellate in the Patellidae and Nacellidae (Stützel, 1984: pl. 3,
ctenidium is plesiomorphic for patellogastropods, for their cteni- fig. C; Fretter & Graham, 1994: fig. 315; Sasaki, 1998:
dium is regarded as homologous with that of other molluscs, on fig. 10f). Because their morphology is discrete, these two charac-
the basis of its position in the pallial cavity, alternate bipectinate ter states may be of phylogenetic significance. Functionally, this
arrangement of lamellae, innervation, blood circulation and organ is assumed to be a sensory organ, tasting the substratum
304ANATOMY OF BATHYACMAEA
Table 1. Comparison of shell and anatomical characters among Bathyacmaea secunda and various patellogastropod families.
Patellidae Nacelldiae Neolepetopsidae Lepetidae Acmaeidae, B. secunda
Lottiidae
Fretter & Graham (1994), Sasaki (1998) Fretter (1990), Angerer & See Table 2 This study
Graham (1964), Stüzel McLean (1990) Haszprunar (1996),
(1984), Sasaki (1998) Sasaki (1998)
Irregular spherulitic Absent Absent ? Present/absent Present/absent Present
prismatic structure
type-A
Semifoliated structure Absent Absent ? Present Present/absent Present/absent
Pallial margin papillae Long Long Short Short Short Short
Pallial sensory stripe Absent Absent Absent Present Absent Absent
Anterior pallial streaks Present/absent Present Present? Absent Absent Absent
Lateral pallial streak Present Absent Absent Absent Absent Absent
Oral lappets Absent Absent Present Present Present/absent Absent
Eyes Present Present Absent Present Present Absent
Ctenidium Absent Absent Absent Absent Present/absent Present
Secondary circumpallial Present, entirely in most Present, except Absent Absent Present/absent‡ Absent
gills species† anteriorly
Osphradia Present Present Absent Absent Present/absent Absent
Radular mineralization Mineralized Mineralized Non-mineralized Mineralized Mineralized Mineralized
Radular formula 3– (1 þ 2) –1 3–2 –1– 2–3 2– (1 þ 2) –1 2– 0–1 –0– 2 2/1/0 –3/1–0 0– 1–0 –1– 0
– (2 þ 1) –3 – (2 þ 1) –2 –1/3–0/1/2
Lateral teeth configuration Inverted V-shaped Inverted Inverted V-shaped – Inverted Inverted V-shaped
V-shaped V-shaped/stepped
Marginal area of radula Broad Broad Broad Narrow Narrow Narrow
Basal plates of radula Present Present Absent Absent Present Present
Sculpture of basal plates Complex Complex – – Simple Simple
Licker Lamellate Lamellate ? Smooth Smooth Smooth
Odontophoral cartilages 3 pairs 5 pairs 3 pairs 2 pairs 2 pairs 2 pairs
Labial cartilages Absent Present ? Absent Absent Absent
Salivary glands Massive, fused Massive, fused ? Tubular, separated Tubular/massive, Tubular, separated
separated
Salivary ducts Two pairs, long Single pair, long ? Single pair, short Absent/single pair, Single pair, short
long
Mid-oesopahgus Torted Torted Not torted Torted Torted Torted
Stomach C-shaped Complex Inverted Inverted C-shaped/complex C-shaped
C-shaped C-shaped/
complex
Intestine 4 loops-complex Complex 3 loops Complex 2 loops-complex 4 loops
Retractor muscles of Ventrally fused Ventrally fused ? Separate Separate Separate
subradular membrane
Median protractor muscles Asymmetrical Asymmetrical ? Symmetrical Symmetrical Symmetrical
of subradular membrane
Median tensor muscle of Present Present ? Absent Absent Absent
radular sac
Median retractor muscle of Present Present ? Absent Absent Absent
radular sac
Efferent pallial vessel(s) Left only Right and left Left only Left only Left only Left only
Intestine and ventricle Not enclosed Not enclosed Not enclosed Not enclosed Not enclosed§ Enclosed by
ventricle
Left kidney and pericardium Adjacent Adjacent Separated Adjacent Separated Separated
Fuchigami & Sasaki (2005).
†
Ridgway et al. (1998).
‡
see Lindberg (1988) for details.
§
except Erginus apicina (Lindberg, 1988: fig. 4k).
305T. SASAKI ET AL.
Table 2. Comparison of shell and anatomical characters among Bathyacmaea secunda and other acmaeids and lottiids.
Acmaeidae Lottiidae
Bathyacmaea Pectinodonta Niveotectura Rhodopetala Erginus Lottia subrugosa Nipponacmea
secunda orientalis pallida rosea sybaritica schrenckii
This study Sasaki (1998) Sasaki (1998) Lindberg (1981) Sasaki (1998) Righi (1966) Sasaki & Okutani (1993)
Irregular spherulitic Present Present Absent ? ? ? Present
prismatic structure
type-A†
Semifoliated structure† Present Present Absent Absent Absent Absent Absent
Irregular crossed foliated Absent Present Absent Absent Absent Absent Absent
structure†
Oral lappets Absent Present Present Present Present Absent Absent
Eyes Absent ? Present ? Present Present Present
Osphradia Absent Absent Absent Present Present Present Present
Ctenidium Present Present Present Vestigeal Absent Present Present
Radular formula 0 –1–0 –1– 0 0 –1– 0–1 –0 0 –3– 0–3 –0 0 –3– 0–3 –0 0– 3–0 –3– 0 1– 3–0 –3– 1 1/0–3 –0– 3–1/0
Lateral teeth configuration Inverted Inverted Inverted Inverted Inverted Stepped Stepped
V-shaped V-shaped V-shaped V-shaped V-shaped
Salivary glands Tubular Tubular Tubular ? Massive ? Massive
Salivary ducts Single pair, Single pair, Single pair, ? Single pair, ? Single pair, long
short short short long
Lateral sublingual Absent Present Absent Absent Absent Absent Absent
pouches‡
Stomach C-shaped Complex Complex C-shaped C-shaped C-shaped C-shaped
Intestine 4 loops Complex Complex 2 loops 4 loops 4 loops 4 loops
Nakano & Ozawa (2004).
†
Fuchigami & Sasaki (2005).
‡
Sasaki (1998).
during grazing (Ponder & Lindberg, 1997: 173– 174). Outgroup their actual food source has not been identified, this remains
comparison suggests that the lamellate type is apomorphic, speculative. The inclusion of mineral grains in the gut contents
because the smooth type is generally found in other basal suggests that B. secunda grazes in the same way as other
gastropods. patellogastropods.
The radular tooth morphology of the genus Bathyacmaea is The salivary glands of patellogastropods are variable and can
unique among patellogastropods in four features: (1) a single be classified into three types by the criteria of form, fusion and
pair of lateral teeth; (2) mineralized trifid cups; (3) long position (Sasaki, 1998). (1) massive fused glands behind the
shafts; and (4) robust basal plates with simple attachment buccal mass; (2) massive but separate glands behind the
scars. Among these, the third character is an autapomorphy of buccal mass; and (3) tubular separate glands along the lateral
Bathyacmaea; the rest are found in some members of the pouches of the anterior oesophagus. The glands in B. secunda
Acmaeoidea. are of type (3), as also found in lepetids and acmaeids.
In spite of striking differences in overall morphology, the The rotation of the oesophagus as a result of ontogenetic
single pair of teeth with trifid cups in Bathyacmaea is comparable torsion has been mentioned in accounts of the comparative
to those of Pectinodonta (Marshall, 1985; Hasegawa, 1997: fig. 2) anatomy of patellogastropods (e.g. Lindberg, 1981), but its sig-
and Serradonta (Okutani et al., 1992: figs 5 –6; Sasaki et al., 2003: nificance is difficult to interpret at present. The degree of
fig. 8D). The radula teeth of these groups are interpreted as a rotation is 180 in B. secunda, but is notably smaller (1358 in
single pair, although they might represent the fusion of three Phodopetala rosea ) or much larger (more than 2508, up to
original pairs of teeth. This structural similarity is one of the 3308) in other patellogastropods (Lindberg, 1981). Further-
arguments for assigning Bathyacmaea, Pectinodonta and Serradonta more, very unusually for basal gastropods, the mid-oesophagus
to the same higher taxonomic group (e.g. Sasaki et al., 2003). of the Neolepetopsidae (Eulepetopsis vitrea ) is not affected at all
Robust and simple basal plates are shared with the Acmaei- by torsion (Fretter, 1990). Because the cross-section of the
dae and Lottiidae and contrast with the thin and sculptured oesophagus has not been described in most previous studies,
plates of the Nacellidae and Patellidae and with the absence of more extensive investigation is necessary to evaluate this
plates in the Neolepetopsidae and Lepetidae. Because other mol- character.
luscs obviously lack homologous plates, the presence of basal The internal structure of the patellogastropod ‘stomach’ is
plates is apomorphic. Thus, this character suggests the relation markedly simplified and lacks some structures common for gas-
of Bathyacmaea with the Acmaeidae and Lottiidae. Functionally, tropods, like the gastric shield and caecum (cf. Sasaki, 1998:
thickened plates may provide mechanical reinforcement of the fig. 99; Strong, 2003: fig. 1). In B. secunda, two regions are recog-
radula during grazing. nized in the stomach, the anterior striated part around the
The function of the long shaft of Bathyacmaea radular teeth opening of the digestive gland (Fig. 5: st1) and posterior
is unclear. One hypothesis is that each tooth is used like a smooth area with thin typhlosoles (Fig. 5: st2). The former
spoon to graze on the surface of the substratum. Because might be homologous with the sorting area of other gastropods.
306ANATOMY OF BATHYACMAEA
The latter may represent a modified style sac or an enlarged The structure of the nervous system in B. secunda is of the
initial part of the intestine, as suggested by Graham (1949) typical patellogastropod type with labial ganglia, labial commis-
and Fretter (1990: 550). sure, a tight visceral loop and completely circular pedal cords
The post-oesophageal configuration of the gut of Bathyacmaea (analogous to those of monoplacophroans: Haszprunar &
is of a simple type for Patellogastropoda. A similar configuration Schaefer, 1996; Schaefer & Haszprunar, 1996). No clear differ-
is known in a number of lottiid species (e.g. Walker, 1968; ences in the nervous system have been detected among patello-
Sasaki & Okutani, 1993; Sasaki, 1998) and some members of gastropods at higher taxonomic levels.
the Patellidae (Sasaki, 1998: fig. 2d). In contrast, the gut is The eyes are absent in Bathyacmaea, as is generally expected for
more complicated in nacellids, lepetids and some acmaeids deep-sea organisms. The absence of eyes is also known in other
(Pectinodonta: Sasaki, 1998: fig. 17d, e; Niveotectura: Sasaki, deep-sea vent-limpets, the Neolepetopsidae (Fretter, 1990). In
1998: fig. 19). As the configuration of gut loops is greatly vari- subtidal lepetids (Lepeta, Iothia and Propilidium ), eyes without
able, it is not possible to establish topological correspondence pigmentation are present (Angerer & Haszprunar, 1996), but
of loops in the complicated type. Ecological correlations of gut the condition in bathyal lepetids is unknown. The degeneration
length and configuration are unknown. of eyes is general among bathyal molluscs (e.g. Sasaki et al.,
The buccal musculature of patellogastropods can be classified 2006).
into patelloidean and acmaeoidean types (Sasaki, 1998) and The osphradia and their associated ganglia are absent on the
that of B. secunda belong to the latter. These two types are floor of the pallial cavity in Bathyacmaea and also in acmaeids,
defined by four characters: (1) the retractor muscles of the subrad- lepetids and neolepetopsids (Fretter, 1990; Angerer & Haszpru-
ular membrane (Sasaki, 1998: character 39); (2) the median pro- nar, 1996; Sasaki, 1998). In ecological terms, it seems that sub-
tractor muscles of the subradular membrane (Sasaki, 1998: tidal and deep-water species lack osphradia. Their absence is,
character 40); (3) the median tensor of radular sac (Sasaki, however, difficult to interpret from a functional viewpoint, as
1998: character 42); and (4) the median retractor of radular sac the primary function of the osphradium has been inferred to
(Sasaki, 1998: character 43). The states in these muscles clearly be sensing and coordinating gamete release for external fertiliza-
support the relation of B. secunda with acmaeoidean groups. tion (Haszprunar, 1985).
One newly observed and unusual state in B. secunda is a thin The isolated lateral position of the statocysts in B. secunda is
single-layered ventral approximator muscle exclusively ventral exceptional among patellogastropods. In the majority of patello-
to the intercartilage connective tissue (Fig. 6D). In other gastropods, the statocysts are attached to the pleural ganglia
groups of patellogastropods, the ventral approximator is thick (e.g. Patella: Stützel, 1984: fig. 15; Cellana: Sasaki, 1998:
and double-layered, intercrossed among connective tissue and fig. 9b; Lottia: Righi, 1966) or outer lateral part of the pedal
more dorsally inserted between paired odontophoral cartilages ganglia (Eulepetopsis vitrea: Fretter, 1990: fig. 6). In B. secunda,
(e.g. Graham, 1964: fig. 13). In more primitive molluscs, such however, the statocysts are separated from these ganglia
as polyplacophorans and monoplacophorans, the homologous (Figs. 13, 14C). This might be comparable to the isolated con-
muscle is thick and medially inserted between the odontophoral dition in monoplacophorans (Lemche & Wingstrand, 1959;
cartilages (Wingstrand, 1985: figs 16, 22, muscle IIIa), as in Wingstrand, 1985; Haszprunar & Schaefer, 1996; Schaefer &
patellogastropods excluding Bathyacmaea. The state in Bathyac- Haszprunar, 1996). The inclusion of many statoconia is a
maea is therefore regarded as autapomorphic. shared character of patellogastropods (e.g. Stützel, 1984: pl. 6,
The position of the left kidney of B. secunda is similar to that of fig. a).
patellogastropods other than patellids, nacellids and lepetids. The
left kidney is separated from the pericardium in the Acmaeidae,
Lottiidae and Neolepetopsidae (Fretter, 1990), but closely abut-
ting in the Patellidae, Nacellidae and Lepetidae (Sasaki, 1998).
Systematic implications
These two types might be correlated with the presence or The anatomical observations in this study have confirmed that
absence of the ctenidium in most members, but the configuration B. secunda belongs to the Patellogastropoda. In addition, it was
of these organs in neolepetopsids (with a separated left kidney, but revealed that some of the diagnostic characters of patellogastro-
lacking the ctenidium; Fretter, 1990: fig. 3) refutes this idea. The pods (Sasaki, 1998: 208) need to be revised. Two exceptional
difference in the position of the kidney is associated with the con- character states were found in the heart and buccal musculature
dition of the renopericardial connections. In the Patelloidea and of B. secunda. The ventricle enwraps the intestine and the ventral
Lepetidae of the closely located type, connections are formed approximator muscle of the odontophoral cartilages is only
with both left and right kidneys. In contrast, in the distantly inserted ventrally and is single-layered. The former has pre-
separated type, the connection exists only in the left kidney, as viously been described only in Erginus apicina (Lindberg, 1988)
in B. secunda. However, the presence or absence of renopericardial and the latter state is a new observation among patellogastro-
connections should be examined more closely in the various pods. These results refine previous knowledge of the patellogas-
groups, because its presence has been insufficiently described in tropod body plan.
the past. In the first author’s experience, the presence of renoper- Within the Patellogastropoda, there are four or three super-
icardial connections can best be determined by the observation of families, namely, the Patelloidea, Neolepetopsoidea, Lepetoidea
opening(s) on the inner wall of the pericardium, in addition to and Acmaeoidea (s.s.), or the Patelloidea, Neolepetosoidea and
longitudinal histological sections. Acmaeoidea (s.l.), including the Lepetidae (Lindberg, 1988,
The structure of the heart in B. secunda conforms to the general 1998; Sasaki, 1998). Among these, B. secunda has been assigned
pattern of patellogastropods, except in one major difference. to the Acmaeoidea, on the basis of the possession of foliated
Part of the ventricle in the pericardium envelops the intestine shell structure, the ctenidium, and the radular teeth made up
in B. secunda, but these are separated in the rest of the patello- of three elements or cusps (Okutani et al., 1993).
gastropods except Erginus apicina (Lindberg, 1988: fig. 4k). The A close association of B. secunda with Patelloidea (Patellidae
ventricle enwrapping the intestine is generally regarded as and Nacellidae) is apparently rejected by the fact that there is
primitive for gastropods by outgroup comparison (Ponder & no uniquely shared character among these groups. In particular,
Lindberg, 1997: 117– 119). Functionally, its significance is the long papillae of the pallial margin and four characters of the
unclear; there is obviously no ecological correlation, because buccal musculature (Table 1) support separation of the Patelloi-
Erginus inhabits the shallow subtidal zone on coralline algae dea within the Patellogastropoda (Sasaki, 1998; see also Nakano
and Bathyacmaea deep-sea chemosynthetic communities. & Ozawa, 2004, for the latest molecular phylogenetic analysis).
307T. SASAKI ET AL.
The possible relation of B. secunda and neolepetopsids is inter- through the kind assistance in sampling by the crew of Shinkai
esting in terms of their common habitat (vents), but actually 2000 and R/V Natsushima and collection management by sup-
there is no uniquely shared character between them. Neolepe- porting staff of JAMSTEC. This study was supported by a
topsids are diagnosed by characters such as the absence of the Grant-in-Aid from the Japan Society of the Promotion of
ctenidium, nonmineralized articulated radular teeth, the lack Science (No. 15740309, 15403014).
of the twisted part in the mid-oesophagus (Fretter, 1990), but
none of these characters is found in B. secunda. Other character
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simple sculpture. The relation of these acmaeoidean groups HASEGAWA, K. 1997. Sunken wood-associated gastropods collected
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has been incompletely resolved, but it is obvious that Bathyacmaea descriptions of 12 new species. National Science Museum Monographs,
has a larger number of similarities with acmaeids (Pectinodonta 12: 59–123.
and Niveotectura: Table 2) than with others. Therefore, we HASZPRUNAR, G. 1985. The fine morphology of the osphradial sense
regard the allocation of Bathyacmaea to the Acmaeidae (sensu organs of the Mollusca. I. Gastropoda, Prosobranchia. Philosophical
Lindberg, 1986) as reasonable. Transactions of the Royal Society of London, B307: 457 –496.
In comparison with acmaeid genera and with other patello- HASZPRUNAR, G. 1988. On the origin and evolution of major
gastropods, the diagnosis of the genus Bathyacmaea is revised as gastropod groups, with special reference to the Streptoneura.
follows: a purely white shell; nearly smooth and heavily eroded Journal of Molluscan Studies, 54: 367–441.
shell surface; shell consisting of five layers (excluding myostra- HASZPRUNAR, G. & SCHAEFER, K. 1996. Anatomy and
cum), i.e. three semi-foliated (M21, Mþ1 and M þ 3) layers, phylogenetic significance of Micropilina arntzi (Mollusca,
concentric crossed-lamellar (M þ 2) layer and irregular spheru- Monoplacophora, Micropilinidae Fam. nov.). Acta Zoologica, 77:
litic prismatic (M þ 4) layer (Fuchigami & Sasaki, 2005); small 315 –334.
pallial-margin papillae; ctenidium present in pallial cavity; LEMCHE, H. & WINGSTRAND, K.G. 1959. The anatomy of
absence of osphradium; smooth licker; two pairs of odontophoral Neopilina galatheae. Galathea Report, 3: 9–71.
cartilages; radular teeth with long shafts and three cusps; LINDBERG, D.R. 1981. Rhodopetalinae, a new subfamily of
radular teeth mineralized (dark brown) only at tips; radular Acmaeidae from the boreal Pacific: anatomy and systematics.
teeth resting on thick, smooth basal plates; acmaeoidean type Malacologia, 20: 291 –305.
of buccal musculature; single-layered ventral approximator LINDBERG, D.R. 1986. Name changes in the “Acmaeidae”. Veliger, 29:
muscle of odontophoral cartilages; simple C-shaped stomach 142 –148.
with four intestinal loops; intestine running through the ventri- LINDBERG, D.R. 1988. The Patellogastropoda. Malacological Review,
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lated from pleural and pedal ganglia. LINDBERG, D.R. 1998. Order Patellogastropoda. In: Mollusca: The
In summary, B. secunda has distant relationships with patelloi- southern synthesis. Fauna of Australia. Vol. 5, Part B. (P.L. Beesley,
deans and neolepetopsids, but is more closely related to acmaeids G.J.B Ross, A. Wells, eds), 639–652. CSIRO Publishing,
in anatomical characters. However, detailed discussion on infrafa- Melbourne.
milial relationships of the Acmaeidae is not possible at present McLEAN, J.H. 1990. Neolepetopsidae, a new docoglossate limpet family
without data on the type species of some related genera from hydrothermal vents and its relevance to patellogastropod
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ing on a larger number of taxa should be made in the future, using MARSHALL, B.A. 1985. Recent and Tertiary deep-sea limpets of the
genus Pectinodonta Dall (Mollusca: Gastropoda) from New Zealand
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ACKNOWLEDGEMENTS biogeography of limpets of the order Patellogastropoda based on
mitochondrial DNA sequences. Journal of Molluscan Studies, 70:
We are indebted to Dr David G. Reid (Natural History 31 –41.
Museum, London), Dr Anders Warén (Swedish Museum of OKUTANI, T., FUJIKURA, K. & SASAKI, T. 1993. New taxa and
Natural History), an anonymous reviewer and Prof. Kazushige new distribution records of deepsea gastropods collected from or
Tanabe (University of Tokyo) for their critical comments and near the chemosynthetic communities in the Japanese waters.
improvement of the manuscript. The material was available Bulletin of National Science Museum, Tokyo, Series A, 19: 123 –143.
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