ON THE REPRODUCTION OF OLIV ELLA
b y Eveline and E rnesto M arcus
(w ith 1 plate)
T hanks to th e O ceanographic In stitu te of th e U niversity of
São Paulo (P rofessor W ladim ir B esnard) we could observe the
reproduction of Olivella w hose fem ale organs are the m ost pe­
culiar of ou r form erly studied olivids. The “N o rth ern B ase”
(Dr. Edm undo N onato) of the m entioned In stitu te p u t its in sta l­
lations a t ou r disposal in the m ost generous w ay.
In the fine sand of th e Enseada n e a r U batuba (23°27’ S. 45°6’
W) O. verreanxii (D ucros 1857) lives in th e zone of th e neap
tides. On October 31st, 1958 th e re w ere about 30 snails p e r sq.
rn. on the surface of th e sand or a little u n d e r it at low tide-tim e.
As the population is dense and th e anim als craw l rapidly, about
10 cm. a m inute a t 24° C., th e m ates m eet easily. W e m aintained
about 300 snails in an enam el tra y of 60 x 40 cm. w ith 1-2 cm.
of sand and equal h e ig h t of w a te r w ith o u t aerification. They
w ere fed w ith living young Donax hanleyanus and crushed
larg e r ones and observed fo r 9 days n early w ith o u t losses. One
or o th er snail w hich craw led out of the tra y d u rin g the night,
and w as found on th e d ry in th e m orning, recovered a fte r a
sh o rt tim e in w a te r. T he accum ulation of the anim als evidently
favoured copulation, because joining began in the afternoon,
about 1 h o u r a fte r the installatio n of the snails.
The position of th e m ates of Olivella during th e act of
coupling (Fig. 2) is not recorded from o th er prosobranchs in
th e com pendia of S im roth (1904), M eisenheim er (1921), A nkel
(1936) and Fischer (1950); in some tectibranchs th e slug th a t
functions as m ale is situ ated behind th e fe m a le .
The m ale stretch es its propodium forw ard like a snout
(Fig. 1, o) and grasps th e upperm ost w horl of th e fem ale’s shell
in its m edian propodial fu rro w (Fig. 2 ). W e rem em b er th a t
190
E. & E. M ARCUS
only in m ales the v en tral propodial fu rro w is distin ct. The
a n te rio r pedal m ucous gland does not seem to tak e p a rt in the
attachm ent, to judge from the fact th a t th e m ates separate
easily a fte r copulation, and th reads or traces of m ucus w ith
adhering sedim ents w ere not left on th e shell of the fem ale.
A reaction of the fem ale w hen th e tip of th e shell was seized
by the m ale w as not observed; both snails continue to craw l a t
the sam e ra te of m otion. E vidently the m ale recognizes the
fem ale by chem oreceptors, perhaps th e propodial sensorial cells,
before it puts fo rth its propodium ; this m ovem ent was n ev er
u n d e rta k en ten tativ ely b u t alw ays followed by seizing the shell
of the snail craw ling in fro n t. As in the previously counted
sam ples the fem ales outnum bered the m ales greatly, so th a t
th ere was no com petition am ong the la tte r. W hile the couple
craw ls, the penis (Fig. 2, p) is protruded, extended forw ard on
the rig h t side, and enters the m antle cavity of the fem ale.
Som etim es a m ale w as seen attached to a feeding fem ale.
R arely th e m ale curved its penis to the left and did not succeed
to e n te r the m antle cavity; usually an in itial curving to the
left w as corrected quickly.
W hen the m ale begins to ejaculate, the fem ale stops moving.
Both m ay be on the surface or half b u rrie d in the sand, or
only th e fem ale is p artially concealed and the m ale rem ains
visible. The m ale je rk s vividly so th a t th e ejaculations can
be counted; we observed up to 16 effected w ith in tervals of a
few seconds. The w hite pellets of sperm are seen passing through
th e tra n sp a re n t penis. Som etim es the ejaculating m ale tw itches
so violently th a t the fem ale is tu rn e d around w ith o u t loss of
the penial and propodial contact. A fter the first 3 hours of
observation, during w hich copulation w as frequent, th e males
seem ed to be ra th e r tired, to judge from th e long duration, up
to 10 m inutes, of the pre-copulatory attach m en t.
Fem ales preserved im m ediately a fte r copulation, dissected
or sectioned, showed pellets of sperm w ith prostatic secretion
betw een the leaflets of the ctenidium . W hile studying the
fem ale organs w e had already found sperm in th e gill of snails
preserved im m ediately a fte r cap tu re. T herefore we conclude
R E PR O D U C T IO N O F O L IV E L L A
191
th a t th e penis does n ot e n te r the opening of the capsule gland
n o r th a t of th e in te rn al vesicle (M arcus 1959, f. 44, iv), b u t
only the m antle cavity.
O. verreauxii does n ot have any
sperm -receiving organ in the o u ter p a rt of its fem ale system .
The receptaculum sem inis (ibid, rn ) lies fa r in w ard betw een
album en and capsule g lan d s. It contains sperm in the sectioned
fem ales th a t w ere p reserved im m ediately a fte r copulation.
P roblably these sperm s do not come from the last b u t from
previous copulations. This is indicated by the stage of the
in tern al vesicle w hich is in the phase of oviposition to be
described in th e follow ing.
T hough sperm atozoa w ere not
seen in the sperm channel of the capsule gland in fem ales
preserved im m ediately a fte r copulation or during and a fte r
deposition of egg capsules, they probably m ake th e ir w ay
actively from th e gill to the receptaculum .
P a ire d m ates separated as softly as th ey join; the m ale
w ithdraw s th e penis and loosens his propodium from the
fem ale’s shell. The m ale m oves aw ay im m ediately, w hile the
fem ale fre q u e n tly rests fo r a short tim e, perhaps due to a mo­
m entary difficulty of resp ira tio n . W hen the eggs a re excluded
from the opening of the m antle cavity th ey are alread y fertiliz ­
ed, and each (Fig. 3, ei) is encased in a capsule ( k ) . T he capsule
passes th rough th e ciliated fu rro w on the rig h t side th a t only
fem ales have into th e v en tral pedal gland as in Nassa m utabilis
(A nkel 1929, f. 1). T here th e capsule is m oulded for about 3
m in u te s. W ith help of a m irro r one can see how th e spherical
capsule is kneaded rap id ly in the cavity of th e gland (Fig. 3).
The in te rn al vesicle contributes to th e form ation of the
capsule w ith its contents and w ith secretion. The faecal p a r­
ticles stored in the vesicle w hich w ere described in ou r first
study of olivids ap p ear in a fine lay er on th e o u ter surface
of th e deposited capsule (Fig. 5 ). These particles a re spread
so sparsely th a t th ey cannot afford any m echanical protection
to th e capsule nor conceal th e em bryo w hich is w hite and
com pletely visible th ro u g h the tra n sp a re n t capsule.
Hence
th e in te rn a l vesicle of O. verreauxii cannot be called a “re in ­
forcem ent sac” as the sim ilar appendage of th e n eritids. no r
192
E. & E. M ARCUS
do its contents constitute an “a rm a tu re ” (A ndrew s 1937, p.
531). Capsules bro u g h t from the beach on a shell w ere quite
clean w ith o u t sand-grains sticking to them , and to those obtain­
ed in the lab o rato ry only occasionally a few grains adhered.
In egg-laying fem ales the cells of th e in te rn al vesicle em it a
secretion of pink staining spherules. This secretion form s a
lay er betw een the epithelium and the faecal particles. The
q u a n tity of th e la tte r dim inishes m easurably during oviposition.
In a fem ale w hich had laid 10 eggs the in tern al vesicle had one
q u a rte r of the volum e of others preserved a fte r copulation
before depositing eggs.
In our opinion the faecal particles and the secretion of the
in te rn al vesicle supply the egg capsule w ith a m a r k . We think
th a t the secretion fastens the particles to the capsule w hen this
leaves the pallial oviduct or capsule gland. The face th a t re ­
ceives the particles w ill be the u p p er p a rt or lid of the deposited
capsule. The la tte r does not have its definitive form w hen it
passes from the opening of th e m antle cavity th rough the
fu rro w on the rig h t side to the m oulding gland. B ut it has a
finely g ran u la r and a sm ooth sticky face. Thus differentiated
it is attached to th e su b stratu m w ith the sticky face and pressed
into the m oulding gland w ith th e face containing the particles.
The folds of the ven tral pedal gland shape the ridges of
the capsule w hich is soft w hen it enters the gland. As Ankel
(1929, p. 224) exposed, the gland functions as a m ould and its
secretion probably hardens the capsule (p. 230). Each capsule
is attached separately and w ith irre g u la r distances from the
others (Fig. 4) to living or em pty Donax, to th e shells of other
Bivalvia (V eneridae), to Bulla striata or to th e glass dish. One
fem ale isolated a fte r copulation produced 6 egg-capsules. in 3
hours, another 13 in 6 hours.
The egg capsule (Fig. 5), a vitreous hem isphere of conchiolin, consists of a rig h t and a left half, firm ly coalesced in a
m edian su tu re as in all capsules of prosobranchs (A nkel 1936,
p. 169). In m any capsules th e m edian su tu re corresponds to
th e g rea ter diam eter. I t extends like a m eridian over th e cap­
sule and corresponds to the sperm channel w hich separates th e
R E PR O D U C T IO N O F O LIV E L L A
193
tw o halves of the capsule gland. F unctionally m ore im portant
is the fu tu re opening of th e capsule, a circular, latitu d in al
lay e r w hich divides th e capsule into an u p p er o percular and
a low er p a rt (Fig. 6). The first is 0,18, th e second 0,12 m m .
h igh. The capsule is broadest at the bottom , viz. about 0,8
mm. The w all of th e bottom , A nkel’s foot plate (1937, p. 77),
is 5 m icra 'thick, th a t of th e u p p e r p a rt 20-40 m icra, and the
lum en 0,5-0,6 mm. w ide. The la tte r contains one egg or em bryo
w ithout “n u rse eggs” b u t floating in album inous liquid ev id en t­
ly furnished by the album en gland.
The w all of th e capsule (Fig. 6) is composed of the sam e
layers as in Nucella lapillus (A nkel 1937, p. 79), an innerm ost
fibrous one, a hom ogeneous layer, one w ith longitudinal and
one w ith radial fib res. The innerm ost and th e hom ogeneous
layers are contiguous, w hile th ey are separated from one an o th er
in N ucella. As b oth stain w ith light-green and th e hom ogeneous
layer is thick, w e suppose th a t th ey derive from the acidophilous
secretion of the g reater, in n e r region of th e capsule gland.
C ertainly th ey correspond to A nkel’s in n e r pellicle and in n er
lay er. These layers can be peeled off from th e o u ter ones.
These are th e m iddel and the o u ter lay e r of A n k el’s term inology.
The longitudinal fibres of th e first, w hich is firm and thin, and
the radial fibres of th e second a re recognizable in clarified
em pty c ap su les. M iddle and o u ter lay e r are basophilous. T he­
refore th e ir origin m ight be traced from th e basophilous se­
cretion of the glands in the sm aller, o u ter region of th e capsule
gland. Also the cem ent w hich attaches th e capsule to th e subs­
tra tu m m ay be a product of th is region. T he faecal particles
from the in te rn al vesicle are em bedded in th e o u ter lay e r of
the operculum .
The opercu lar b o rd er is probably produced by th e blue
staining glands w hich a re disposed in two antero-posterior
stripes opposite to one an o th e r in the m iddel of th e in n er region
of th e capsule g la n d . The lim iting lay e r betw een lid and low er
p a rt of the capsule is g radually dissolved and th e en tire
lid falls off (Fig. 4) w hen th e veliger h atches. T he surface of
th e operculum is sculptured w ith about 5 m icra high raised
194
E. & E. M A RCUS
lines w hich a re 20-30 m icra d istan t from one an o th er (Fig. 46). T hey ru n m ore or less p arallely to the m edian su tu re and
th e ir course is w rin k led by the radial fibres of th e outer lay er
disposed tra n sv e rse ly to th e ridges. The la tte r are united at
th e ir ends generally form ing a rig h t angle w ith th e su tu re.
B ut if th e capsule h ad lain obliquely in the m oulding pedal
gland, th e direction of the ridges is n o t correlated w ith th a t of
th e m edian su tu re . This su tu re continues over th e low er p a rt
of the capsule (Fig. 6). H ere th e ridges are circular, parallel
to those of th e lid, b u t stra ig h t not w rinkled, though radial
fibres are p rese n t also here in the o uter lay er of the w a ll. The
bottom of th e capsule is sm ooth and consists of in n e r fibrous
layer, hom ogeneous layer, and cem ent.
We w ere not in terested in the cleavage and the early de­
velopm ent in the p rese n t stu d y . The eggs are rich in yolk as
those of o th er Stenoglossa. Hence the m icrom eres occupy a li­
m ited and concentrated area over the m acrom eres (cf. Pelsen eer 1906, p. 24). The two and four blastom eres resulting from
the firs t and second cleavage respectively are of equal size.
Thus segm entation corresponds to the C repidula-type; a yolk
sac (A nkel 1936, p. 182) or polar lobe (K orschelt 1936, p. 869)
does not occur.
In o rd er to observe the em bryos and obtain th e larvae the
egg capsules w ere isolated in sm all p e tri dishes. T he tem p era­
tu re w ill not have deviated m uch from th e n a tu ra l condition,
w here it is colder a t n ig h t and w arm er w hen low tides coincide
w ith sunny days. The oxygen supply in th e dishes how ever
differed w idely from the thoroughly aerified superficial layer
of th e sand in th e zone of the neap tides w h ere th e snails liv e .
T herefore ou r data concerning the d u ratio n of th e em bryo’s
life in th e capsule and th a t betw een hatching and m etam or­
phosis only illu stra te th e plasticity of these processes and cannot
De considered averages. The em bryonal developm ent lasted 89 days. T he em bryo began to ro tate on the 3rd day and had a
sm all b ip a rtite velum on th e 4th. Some veligers m etam orphosized 2 hours a fte r hatching (Fig. 14), others had a free living
stage of about a w eek. To judge from its behaviour in our
R E PR O D U C T IO N O F O LIV E L L A
195
dishes th e velig er is not pelagic, b u t swim s a t the bottom . It
lives upon its yolk (Fig. 13, y) and evidently does not feed.
The new ly hatched veliger (Fig. 9) has a quite colourless
shell (Fig. 7; 9, x) w ith o u t any sculpture as it occurs in Buccinum (D akin 1912, f. 64; P o rtm a n n 1925, f. 7) and m any o ther
prosobranchs (V estergaard 1935, f. 2, 5, 7A; T horson 1946, f.
104 A, 130 C, 137 C-F; Rasm ussen 1951, f. 8, and o th e r s ) . The
w idth of the shell is 0,4 mm., its heig h t 0,32 m m . The large
velar area bears two sh o rt tentacles and black eye spots (Fig.
11, z); the cells of the velum (v) contain brow n pigm ent. T he
statocysts (Fig. 13, t) lie in the region behind the velum . Co­
loured larval kidneys are not developed nor could we find such
organs (P o rtm an n 1930) in the sections. The nuchal sinus (P elseneer 1906, p. 135) or larval h e a rt (D akin, 1. c., f. 64, P ul) is
recognizable (Fig. 9, e) dorsally to th e velum a t the m antle
border (Fig. 13, m i) . Its m uscle fibres ap p ear in the sections,
but the organ th a t visibly beats in th e veliger is th e definitive
h e a rt (Fig. 9, h) w hich lies beside the kidney (Fig. 13, n ) . Also
the organs of the pallial cavity (1), a volum inous osphradium
(r), a ctenidium (b) w ith 6 or m ore leaflets, and a h ypobranchial gland are developed. The ganglia of the central nervous
system (c, d) are alread y connected w ith one another, even
th e roots of the visceral loop (su, u) are un ited w ith the pleural
ganglia. The la tte r do n o t lie in the plane of th e section d raw n
in Fig. 13. T he propodial ganglia (ro) begin to em it n erves
into the foot, w hose propodium (o) is delim ited by a constriction
and provided w ith an a n te rio r gland ( g ) . T h ree days a fte r
hatching the parapodial flaps (Fig. 11, q) are d istin ct. T he
stom ach (Fig. 13, so) and th e tw o sacs of th e digestive gland
are in open com m unication w ith th e yolk (y) w hich in th e
living veliger conceals th e colum ellar m uscle ( w ) . T he fore-gut (i) and th e in testin e are sim ple tu b es.
RESUMO
O livella verreauxii (D ucros 1857) foi criada no laboratório
da Base N orte (Dr. Edm undo N onato) do In stitu to O ceanográfi-
196
E. & E. M A RCUS
c o . Cópula, ovipostura, e la rv a foram d e sc rita s. Os esperm ato­
zóides ejaculados foram encontrados e n tre os folhetos b ra n ­
quiais, de onde sobem p a ra o receptáculo sem inal. Os grumos
fecais arm azenados n a vesícula in te rn a da fêm ea são grudados
no opérculo da cápsula ovular por secreção da vesícula. Está,
d estarte, m arcada a face dirigida p a ra a água por finos grânulos
e diferenciada da face lisa cim entada ao s u b s tra to .
REFERENCES
F o r lite r a tu r e see o u r p a p e r in th is B u lle tin (M arcu s, E. & E.
1959) an d add:
A N K E L , W. E. 1937, D er fe in e re B au des K o k o n s d e r P u rp u rsc h n e c k e
N u ce lla la p illu s (L.) u n d seine B e d eu tu n g f ü r d as L aichleben.
Zool. A nz. S uppl. v. 10 (V erh. D. Zool. Ges. 1937), p. 77-86,
12 te x t-fig s . L eipzig.
K O R SC H E L T , E. 1936, V erg le ich e n d e E n tw ic k lu n g sg e sc h ic h te d er
T ie re (K o rsc h e lt & H eid er, n ew ed .), v. 2, p. 537-1314, f.
561-1312. J e n a (G. F isc h e r).
M E ISE N H EIM E R , J . 1921, G esch lech t u n d G esc h le ch te r im T ierreich e,
v. 1. X IV + 896 p., 737 te x t-fig s . J e n a (G. F is c h e r).
P E L S E N E E R , P. 1906, M ollusca. E. R ay L an k e ste r, A T re a tise on
Z oology, pt. 5, 355 p., 301 figs. L o n d o n (A d am & C harles
B la c k ) .
P O R T M A N N , A. 1925, D er E in flu ss d e r N ä h re ie r a u f die L a rv e ­
n e n tw ic k lu n g v on B uccinum u n d P u rp u r a . Z eitsch r. M orphol. O ekol. v. 3, fase. 4, p. 526-541. 18 te x t-fig s . B e rlin .
PO R T M A N N , A. 1930, D ie L a rv e n n ie re n v o n B u ccin u m u n d a tu m .
Z eitsch r. Z ellforsch, m ik r. A n at. v. 10, fase. 2, p. 401-410,
te x t-fig s . 1-10. B e rlin .
R A SM U SSEN , E. 1951, F a u n istic an d B iological N otes on M arine
In v e rte b ra te s . II. V id en sk . M eddel. D an sk N a tu rh . F oren,
v. 113, p. 201-249, 29 te x t-fig s . K ö b en h a v n .
T H O R SO N , G. 1946, R e p ro d u c tio n an d la rv a l d ev e lo p m e n t of D an ish
m a rin e b o tto m in v e rte b ra te s . M edd. K om m . D anm . F isk . &
H a v u n d e rs. ser. P la n k to n v. 4, n.° 1, p. 1-523, 196 figs.
K öbenhavn.
V E STER G A A R D , K. 1935, U eb e r d en L aich u n d d ie L a rv e n von
S c a la ria com m unis (L a m .), N assariu s p y g m a eu s (L am .) u n d
B ela tu rric o la (M o n t.). Zool. Anz. v. 109, fasc. 7-8, p. 217222, 7 te x t-fig s . L eipzig.
PLA TE
PLA TE 1
Olivella verreauxii
Fig.
Fig.
Fig.
Fig.
Fig.
Fig.
Fig.
Fig.
Fig.
Fig.
Fig.
Fig.
Fig.
Fig.
1 —
2 —
3 —
4 —
5
6
7
8
9
10
11
12
13
14
M ale scenting fem ale.
M ating couple.
Fem ale m oulding cap su le.
Shell of Donax w ith 3 capsules and an em pty lower
p a rt.
—
Egg capsule.
—•
Section of sam e.
—
Shell of veliger.
—
O perculum of sam e.
—
N ew ly hatched veliger, dorsal view .
—
V entral view of sam e.
—
T hree days old veliger, dôrsal view .
—
V entral view of sam e.
—
Sagittal section of veliger.
—•
R ecently m etam orphosized snail.
a — anus, b — ctenidium . c — cerebral ganglion, d —
pedal ganglion, e — larval h e a rt, ei — egg. f — foot, g — foot
g la n d . h — definitive h e a r t. i — fo re -g u t. j — opercu lu m . k
— egg capsule. 1 — m antle cavity, m — m outh, m i — m antle
b o rd er, n — k idney, o — propodium , p — penis, q — parap o d iu m . ro — propodial gan g lio n . s — sip h o n . so — stom ach.
su — supra-intestinal ganglion, t — statocyst. u — subintes­
tin a l ganglion, v — velum , w — colum ellar m uscle, x — shell,
y — yolk, z — eye.
E. & E. M A RCUS — O L IV E L L A — P L A T E 1