Marine Biology 101,227-233 (1989) Marine

..... B i o l o g y
.__.--
9 Sp~ng~-Vorb~ 19e9

Life history of the golden ring cowry Cypraea annulus

(Mollusca: Gastropoda) on Okinawa Island, Japan

M. Katoh *

Department of Marine Sciences, University of the Ryukyus, Nishihara, Oldnawa 903-01, Japan

Abstract ies on the life histories of cypraeids have reported only

spawning behaviors, fecundity, and morphology of veligers
TWo mark-recapture studies, regular population censuses, (e.g. Ostergaard 1950, Natarajan 1954, 1957, D'Asaro 1970,
field observations, and laboratory culture were used to Renaud 1971, Bandel 1973, Taylor 1975, Tanaka 1980).
study the life history of the tropical marine gastropod Cy- Only one paper (Darling 1965) dealt with juvenile growth
praea annulus Linnaeus, 1758 from Cape Maeda, Okinawa (on Cypraea cinerea). Little is known of the growth and
Island, from April 1984 to March 1986. In the field, the reproduction of the common intertidal cowry C. annulus
average rate of increase in shell length of marked juvenile Linnaeus, 1758 in the Indo-West Pacific. Only a few field
snails was 1.0 • mm w k - 1 ( N = 13), with a maximum of studies have been carried out on adult growth and male and
1.5 mm w k - 1 (initial shell length 10.6 to 17.2 ram). In the female size in C. annulus (identified equivalently as Moneta-
laboratory, the maximum growth rate of juveniles was ria annulus). At Heron Island, Australia, Frank (1969)
3.0 mm w k - 1 with food ad libitum. Snails with primordial proved growth of M. annulus to be determinate by mark-
teeth on the shells grew at a rate of 0.1 to 0.5 mm wk -1 for recapture censuses. Female C. annulus are usually slightly
about 2 wk. The adults continued to grow at a similar rate larger in shell length than males (Orr 1959, Schilder and
for an additional 3 to 6 wk, and ceased detectable growth Schilder 1961).
when some females started spawning egg masses. In the The purpose of the present study was to examine sexual
littoral zone on Okinawa Island, snails reproduced through- maturity, growth, breeding seasons, reproductive behaviors,
out the year. Egg masses brooded by three females (shell fecundity, frequency of spawning, and male and female size
length 17.4 to 21.3 ram) in the field contained 90 000 to in the golden ring cowry Cypraea annulus.
133 000 ova. In the laboratory, brooding periods of three
females lasted 6, 8, and 9 d. The estimated average frequency
of spawning was 5 egg masses female-1 yr-1. The mean Materials and methods
shell length of adult females (20.3 ram) was significantly
larger than that of adult males (19.6 ram). The life-history The study site was located on an eroded limestone platform
strategy of C. annulus is characterized by rapid growth, high (ca. 20 to 70 m wide) of a fringing reef at Cape Maeda on
fecundity, and repeated spawning throughout the year.
Okinawa Island, Japan. Four small coves were chosen for
the experiments (Fig. 1). The substratum consists of coral
and limestone, and is usually exposed at low tide, except in
tide pools. Wave action at the study site is mild during most
Introduction
of the spring and summer, except for the periods of occa-
sional typhoons, but is harsh during most of the fall and
The life histories of few tropical marine gastropods have winter because the site faces the dominant NW monsoon
been studied (e.g. Frank 1969, Kenny 1977, Yamaguchi
wind. One typhoon passed within 300 km of Okinawa Is-
1977, Perron 1983, 1986, Burgett et al. 1987, Smith 1987). land in August 1984 (Okinawa Meteorological Agency
The family Cypraeidae especially has received little atten- 1985).
tion from scientists interested in life history strategies. Stud-
Three developmental stages after settlement were distin-
guished in Cypraea annulus Linnaeus, 1758 according to
* Present address: Department of Zoology and Physiology, Loui- shell morphology (Fig. 2). The S1 stage begins at completion
siana State University, Baton Rouge, Louisiana 70803-1725, USA of metamorphosis. Kay (1985) called this stage an oliviform
228 M. Katoh: Life history of Cypraea annulus

127"q0'E leased within 4 h. Snails painted at each census were distin-

I I
OK
N
IA):W
,C : A
~ guished by different colors. Six biweekly censuses were
....... * made, during which period 32 out of 198 marked cowries
26o40, N were recaptured. Growth was measured as the difference
between the original and the present shell length, from the
PACIFIC apex to the farthest point of the outer lip (Yamada 1987).
Seventeen S1 snails, collected from May to July 1984,
m were reared in laboratory aquaria until December 1984.
UNIV, RYUKYUS Seawater temperatures varied in accordance with room tem-
perature (21 ~ to 29 ~ The cowries were fed fresh filamen-
j l J 26~ tous green algae (e.g. Enteromorpha intestinalis) from May
Fig. 1. Cape Maeda, Okinawa Island, Japan, showing locations of to July. Since the fdamentous algae were not found in situ
stations after July, the preserved brown alga Undaria pinnatifuta was
given thereafter. Shell lengths of the S 1 snails were measured
weekly from May to September 1984.
Size-frequency distributions of S1 and $2 snails were
ascertained in 22 biweekly or monthly samples between June
1984 and July 1985 at Coves 1 and 4. Samples 1 to 5 were
made at Cove 4. No S1 snails were found in Sample 6 at
Cove 4 because the cove was completely exposed during the
summer midday low tides and the density of the snails had
been reduced by a typhoon. Samples 6 to 18 were therefore
made at Cove 1, which was less exposed.
$3 snails ( N = 676) were marked with small numbered
tags attached to the dorsal surface of their shells with a
fast-drying adhesive at Cove 1 between June and August
1984, for mark-recapture studies used to examine the pat-
tern of growth.

Breeding season

Counts were made of the number of snails sitting on egg

masses, or "brooding" snails, during monthly 15 min
searches at low tide from June 1984 to July 1985. The brood-
ing snails were considered mature females, since all 13 col-
Fig. 2. Cypraea annulus, Shell morphology of three developmental lected at Cape Maeda were confirmed to be female by dissec-
stages. Top: dorsal view;, bottom: ventral view. 1: $3, adults with
tion. Furthermore, spawning females brooded their egg
complete rings on dorsal surfaces; 2: $2, snails with primordial teeth;
3: St, juveniles masses in aquaria. Size-frequency distributions in growth
studies were also used to determine seasons of $1 snail re-
crnitment.
or "bulla" stage. The $2 snails have primordial or develop-
ing teeth on the shell aperture. The $3 stage is recognized by
the completion of a bright orange-yellow ring on the dorsal Fecundity
surface.
Three brooding females and their brooded egg masses were
collected from Cove 3. The number of egg capsules per egg
Growth mass and the number of eggs per capsule from ten haphaz-
ardly chosen capsules were counted. Heights and widths of
Two mark-recapture studies of S1 and $3 snails, laboratory the ten capsules were measured under a profile projector to
cultatre, and regular population censuses were used. The the nearest 0.1 ram.
shell lengths were measured to the nearest 0.1 mm with ver-
nier calipers. Shell widths and heights were also measured in
the mark-recapture studies of $3 snarls. Spawning frequency
Mark-recapture studies of $1 snails were carried out
from May to August 1984 in Cove 4 to determine growth The spawning cycle of snails that brood eggs and reproduce
rates. On each date, 19 to 51 S1 snails were collected, their without synchronization has the proportional relationship:
outer lips were painted with nail polish, and they were re- (average no. of brooding females)/(total no. of fe-
M. Katoh: Life history of Cypraea annulus 229

20

E
E
"!-
I- 15
0
z
u.I
._1
_1
...I
LU
"1- 10 y : : FEMALE
O0
Fig. 3. Cypraea annulus. Individual shell
growth in laboratory from May to September
1984. Shell length plotted as function of time;
Stage $3 commences at Time 0. *: beginning of
I I I 1 Stage $2; B: brooding
-5 0 5 10
TIME (wk)
Table 1. Cypraea annulus, Growth rates (~, mm wk t) of three snails were dissected and sexed by the presence of penises.
developmental stages in field and in laboratory. N: no. of snails. A N O V A was used for size comparison. Correlation coeffi-
- : no data d e n t s between mating male and female sizes were calcu-
Stage Field Laboratory lated.
~? SD N s SD N
Results
S1 1.0 0.3 13 1.3 9 0.7" 5
S1 -$2 0.7 0.4 10 - - -
S1 -$3 0.3 1 - - Sexual maturity
$2 - - - 0.3 0.1 7
$3 0.1 b 0.1 b 12 0.2 c fit ~ 7r Neither b r o o d i n g nor copulating Stage $1 Cypraea annulus
0.0 d~ 0.0 do 6d
were found during the study periods. However, a few copu-
= Excluding first week of observations lating snails of the late $2 stage were observed in the field.
b mm yr- 1 M o s t copulating snails a n d all b r o o d i n g females were at the
c First 6 wk $3 stage. Snails, therefore, become m a t u r e at the late $2
d Subsequent 4 mo
stage.
m m (4 too) 1

Growth
males) = (brooding period)/(period o f spawning cycle).
Thus, the average period o f the spawning c y c l e m a y be Cypraea annulus grew very rapidly during the S1 stage in
indirectly estimated from the first three variables. The aver- both the field and the laboratory, but growth declined with
age number o f b r o o d i n g females and total number of $3 increasing stage (Table 1). In the field, 21 of 198 m a r k e d S1
snails were obtained by monthly 15 rain searches in breeding juveniles were recaptured as SI juveniles, 11 as $2 snails, and
season studies. The sex ratio was not significantly different 1 as a $3 adult. Eight o f these S1 juveniles and one $2 snail
from 1 : 1 in the field. H a f t of the total number o f $3 snails displayed unusually thick rims compare to the n o r m a l thin
were considered female. The b r o o d i n g period was measured juvenile shell. Their growth rates were less than 0.3 m m
in the laboratory. wk-X; the nail-poLish m a r k i n g m a y have disturbed shell
growth. These snails were excluded from the calculations. In
the laboratory, the juveniles' growth declined considerably
Male and female size one week before they became $2 snails (Fig. 3), as the labial
edges began to extend t o w a r d the columellae. The m a x i m u m
The size o f male and female snails was measured on mating growth rate of the $1 stage in the l a b o r a t o r y was 3.0 m m
pairs and b r o o d i n g females collected on 17 April 1984 at wk -1 shell length. One S1 juvenile grew from 10.6 to
Coves 3 and 4, m a t i n g pairs on 4 M a y 1984 at Coves 3 and 18.6mm in 4 wk (i.e., 2 . 0 r a m wk-~).
4, and $3 snails collected h a p h a z a r d l y on 26 M a r c h 1986 at $2 snails grew at reduced rates o f 0.1 to 0.5 mm w k - 2,
Cove 2. M a t i n g snails were easily sexed by the presence of and advanced to the $3 stage in a b o u t 2 wk. After growing
a penis which retracted when a male was disturbed. The $3 into $3 adults with rings on their dorsal surfaces, the adults
230 M. Katoh: Life history of Cypraea annulus

m $I 10
f'Is2 5
0

1(3
5
0
10
5
10
0

Aug. 11

O" mm, , Apr. 23

rm n

"2, O-
t Aug. 28

, I-I,
10
O" | i

0
5
0
5

o
z 5
l
0
lO

10

9 0

10

10 0
5
0 35
30 1984
duly 27 ~g. 4. Cypraea annulus. Size-frequency distribu-
I0 25 tions of $1 juveniles and $2 snails from June 1984

J
5 20 to July 1985 and $3 adults in July 1984 at Cape
0 15 Maeda, Okinawa Island. $2 snails were collected
I051 1985 I0
less extensively on 29 June and 12 July 1984. Site
Jan. 9 sampled on June to August 1984 was approx.
mmm m r~L, 5
150 m away from other site
0~ ~ l~ 15 zb 00 lb 1'~ z'0 2'5
SHELL LENGTH(M) SHELL LENGTH(ram)

continued to grow at a rate similar to that of $2 snails for one exception on 26 September 1984. Because of continuous
an additional 3 to 6 wk, thickening their shell and increasing juvenile recruitment, growth rates could not be estimated
their width during this period. During the subsequent 4 mo from these histograms. The minimum and maximum shell
observation, these shells did not grow detectably in length, length of S1 juveniles collected were 2.5 and 22.5 ram, re-
width, or height (Table 1). TWo females spawned 4 and 5 wk spectively.
after completion of the rings on their dorsal surfaces
(Fig. 3).
Twelve of 676 tagged $3 adults were recaptured 9 to 21 Breeding season
mo after release in the field. Five had grown 0.2 to 0.4 mm
in shell length, while the other seven had not increased more Brooding females were observed in the field throughout the
than 0.1 mm in size. Eight of the recaptured adults had been study period (Table 2). Each search revealed the presence of
marked more than one year earlier. All recaptured snails both yellow and violet egg masses. Violet egg masses appear
had pale, or pale and irregular dorsal surfaces with fading to be older than yellow ones, since egg-mass color changed
rings (perhaps as a result of erosion). from yellow to violet during the brooding period in the
Fig. 4 shows size-frequency distributions of $1, $2, and laboratory aquaria. Juveniles were collected throughout the
$3 snails from June 1984 to July 1985. The size-frequency of year (Fig. 4). Therefore, the population of Cypraea annulus
S1 juveniles in each sample displayed a similar distribution at Cape Maeda reproduced throughout the year without
pattern without distinct modes throughout the year, with detectable peak periods in its breeding activity.
M. Katoh: Life history of Cypraea annulus 231

Table 2. Cypraea annulus. Number of brooding females found dur- Spawning frequency
ing 15rain search at Cape Maeda from June 1984 to July 1985.
During each search, about 190 snails were examined The average brooding period in the laboratory (7.67 d) was
Date No. used for calculations. The average number of $3 adults
found during a 15 min search for brooding females at Cape
1984 Maeda was 187. With a sex ratio of 1 : 1, half (93.5) would
June 28 6 be females. The mean number of monthly brooding females
July 27 14
August 27 8 was 9.85 excluding the months of December 1984 and Feb-
September 25 9 ruary 1985 (Table 2). Thus, the average spawning-cycle
October 26 15 period = 7.67 x 93.5/9.85 = 72.8 d, and the average spawning
November 23 8 frequency = 365/72.8 = 5 egg masses female- a y r - 1.
December 19 2"
1985
January 9 7 Male and female size
January 20 3
February 8 39
March 27 17 At Cape Maeda, the mean shell lengths of females were
April 23 5 significantly larger than those of males between mating pairs
May 22 9 on 17 April 1984 ( F = 13.75; d f = 1, 52; p<0.001) and on 4
June 18 14 May 1984 ( F = 5.88; d f - 1 , 76; p<0.05), and between hap-
July 2 11
hazardly collected $3 snails on 26 March 1986 (F=4.58;
On these dates, searches lasted less than 15 rain d f = l , 191; p<0.05) with a considerable overlap of the
ranges (Table 3). The mean shell lengths of mating and
brooding females on 17 April 1984 were not significantly
Table 3. Cypraea annulus. Shell length of mating pairs, brooding different ( F = 0.22; d f = 1, 50; p > 0.05).
females, and adults at Cape Maeda, Okinawa Island. N: no. of snails
Correlation between sizes of mating males and females
Snails N Mean SD Range were not significant ( r = - 0 . 0 9 4 , df=25, p>0.05 on 17
length (ram) April 1984; r=0.021, df=37, p > 0 . 0 5 on 4 May 1984).
(rnm)

17 April 1984
Mating males 27 18.3 2.36 14.9-23.8
Mating females 27 20.4 1.81 16.8-24.1
Brooding females 25 20.1 2.17 15.0-23.6 Growth
4 May 1984
Mating males 39 17.9 2.30 14.8-22.2 A juvenile Cypraea spadicea grew rapidly at 3.3 mm wk-1 ill
Mating females 39 19.2 2.31 14.5-22.5 an aquarium, except for no growth during the first 2 wk
26 March 1986 (Darling 1965). This rate is similar to the maximum growth
Males 88 19.6 1.80 15.2-23.0 rate of S1 juvenile C. annulus in the aquaria in the present
Females 105 20.3 2.30 15.4-26.7 study, although the adult size of C. spadicea (shell length
45 ram) is about twice that of C. annulus. Snails may en-
hance their fitness by rapid growth with fragile, thin, juve-
Reproductive behavior and fecundity nile shells or by slow growth with strong, thick, juvenile
shells; C. annulus choose the former.
One female Cypraea annulus spawned single egg capsules In my laboratory observations, the juveniles grew more
successively in August in a laboratory aquarium; complete slowly during the first week after introduction into the aqua-
spawning took ca. 24 h. Within 5 d of spawning, the color of ria than in subsequent weeks. Yamaguchi (1975) noted that
the egg mass changed from yellow to violet, the color change young juveniles of many marine sedentary invertebrates
at the center of the egg mass occurring earlier than that at grow slowly, and fitted their growth to logistic rather than
the periphery; veliger larvae emerged after 8 d. The brood- to yon Bertalanffy growth equations. Both juveniles intro-
ing periods of two other females were 6 and 9 d in October duced into the aquaria were not young (C. spadicea, 30 ram);
and December, respectively. Veligers emerged both in the therefore, both Darling's (1965) and my results may be at-
morning and in the afternoon. The females nipped and tore tributable to differences between laboratory and field condi-
off the egg capsules whilst the veligers emerged and, after tions rather than to slow growth of young juveniles.
emergence, moved away and left the emptied capsules on Frank (1969) remarked that growth of Cypraea annulus
site. The size of veligers was 0.13 mm one day after ceased once they reached their adult shape, except for re-
emergence from the egg capsules. pairs to the shell. His growth comparisons, however, were
Egg masses brooded by three females (shell length: 17.4, based not on shell length but on the distance between notch-
21.3, and 20.1 ram) in the field contained 90 000, 127 000, es at the top and bottom of the aperture. In my field study,
and 133 000 ova, respectively. six out of the twelve recaptured $3 adult cowries had ob-
Table 4. Cypraeidae. Life-history data. - : no data

Species Capsule size Capsules/ Eggs/ Eggs/ Days/n Size at Month(s) of Locafity Source
(ram) egg mass capsule egg mass capsula emergence breeding
(um)

Cypraea annulus 0.9 2.0x 233-267 230 603 90000- 6-9 130 b All months* Okinawa Present study
0.7 1.3 133000
20 000 130 O c t . dg Hawaii Ostergaard (1950)
C. caputserpentis 2 100 200
1.1 x 0.9 100-200 200 20 0 0 0 - 18 100-120 All months* Hawaii Kay (1960)
40OOO
5OO000 14 220 J u l y df Hawaii Ostergaard (1950)
C. carneola 4 1 000 500
C. cinerea 2.0-2.5 • 1 400 200-300 J u n e - July a g Colombia and Bandel (1973)
Curacao
C. errones 1.45-3.25 • 481 546 20 76 373 Sep.-MaxY India N a t a r a j a n (1957)
(as Erronea errones) 1.40-1.80
C. fimbriata - - M a r . - O c t . "* Hawaii Taylor (1975)
C. helvola 2 1 000 200 200 000 140 July d, Hawaii Ostergaard (1950)
J u n e - J u l y ~* Hawaii Taylor (1975)
C. isabella 1.5 1 500 200 300 000 11 150 July df Hawaii Ostergaard (1950)
All m o n t h s " g Hawaii Taylor (1975)
C. mauritiana 4x 3 300 ~ 1 003 235 ~ June d f Hawaii Ostergaard (1950)
C. moneta 2.20-3.00 34 596 500 17000- 14 145-155 Eniwetok Renaud (1971)
298 000
C. poraria 140 May d* Hawaii Ostergaard (1950)
C. rashleighana - - - June ~* Hawaii Taylor (1975)
C. spurca acicularis 2.6 x 1.6 140 and 290 1 100 154000 and M a y - J u n e af Florida D'Asaro (1970)
319000
C. teres May ** Hawaii Taylor (1975)
C. vitellus 2.5 • 1.5 380 600 228 000 12 190 July d fB Japan Tanaka (1980)

" Portion of an egg mass

b One day after emergence of veligers
Unsuitable culture conditions
d Month(s) of observation O
~ Month(s) of occurrence of free-swimming veligers
f In vitro
* In situ

r~
M. Katoh: Life history of Cypraea annulus 233

viously increased in shell length, width, and/or height Island (Nakamura 1984). The brooding period in C. annulus
by>0.1 mm b u t < 0 . 7 mm during a period of about 9 to 21 may therefore vary considerably with season.
mo. These individuals apparently continued to grow as Five females in the aquaria spawned three to four times
adults with dorsal tings. In the laboratory, however, there each between July and November 1984 under ad libitum
was no detectable growth during the last 4 mo of adulthood, food supply, equivalent to seven to ten times per year. High
the $3 stage. It would seem, therefore, that the six $3 adults water-temperature and high food-availability may have
which had increased in shell length when they were recap- caused these high frequencies, which are significantly higher
tured had been tagged within 6 wk after completion of their than the estimated frequency of five times per year in the field.
dorsal rings. Consequently, the growth of C. annulus ap-
pears to be determinate.
Male and female size

Breeding season Although he did not compare the difference statistically, Orr
(1959) showed that shell length of female Cypraea annulus in
Cypraea annulus reproduces all year around at Cape Maeda. Zanzibar was slightly larger than that of males, with a con-
At Heron Island, Frank (1969) found egg masses of C. siderable overlap. On the other hand, in the central Pacific
annulus (as Monetaria annulus) in March, June, and July, (the Ellice Islands to the Marshall Islands) and in the Indian
and juveniles from July through February. Egg masses and Ocean (Mahr, Seychelles), Schilder and Schilder (1961)
juveniles might have been difficult to find at Heron Island found that the shells of female C. annulus were not signifi-
because of the lower population density of snails (0.4 m - 2; cantly larger than those of males (p > 0.2). However, their
Frank 1969). C. annulus at Cape Maeda (32.7m-Z; own data for specimens from these different localities were
personal observation) were about 80 times as dense as at pooled, and may have obscured the actual, regional size-
Heron Island. Judging from the occurrence of egg masses differences, between the two sexes. In the present study, the
mean shell length of females was significantly larger than
throughout the year, Kay (1960) suggested that there was no
pronounced breeding season for C. caputserpentis in that of males, with a wide range of overlap.
Hawaii. Taylor (1975) also found planktonic veligers of C. Schilder and Schilder (1961) reported similar results for
isabella throughout the year in Hawaii. On the other hand, Cypraea moneta (as Monetaria moneta) and C. helvola (as
Natarajan (1957) showed that the breeding season of C. Erosaria helvola). Griffiths (1961b) reported female C.
errones (as Erronea errones) in India was from Sep. to angustata to be significantly larger than the males, while
March. Taylor (1975) noted that the greatest diversity and differences in C. errones were not significant. Gri/tiths
abundance of cypraeid larvae in plankton occurred during (1961 a), however, found that the mean shell length of the
the spring and summer in Hawaii. females was significantly less than that of the males in C.
hesitata (as Umbilia hesitata). It appears, therefore, that in
Cypraeidae females are not always larger than males.
Reproductive behavior and fecundity No correlation was observed between sizes of mating
male and female Cypraea annulus. Pairing in C. annulus
Brooding behavior has been reported for many Cypraea would therefore appear to be random with respect to size. To
species: e.g.C, isabella and C. helvola by Ostergaard (1950), my knowledge, no such observation has previously been
reported for the Gastropoda.
C. errones (as Erronea errones) by Natarajan (1954, 1957),
C. spurca acicularis by D'Asaro (1970), and C. viteltus by
Acknowledgements. I would like to express my appreciation to M.
Tanaka (1980). In the present study, female C. annulus were Yamaguchi and S. Katoh for their support and encouragement
also observed brooding their egg masses. throughout this study and for their helpful comments on the ma-
Table 4 shows that the number of capsules per egg mass nuscript. I am grateful to M. Horikoshi and M. Nishida for their
and number of eggs per capsule in Cypraea annulus, C. helpful discussions. The manuscript has also benefited from reading
by K. M. Brown, D. W. Foltz, J. M. Lawrence, K. J. Lupardus, M.
moneta (Renaud 1971), and C. vitellus (Tanaka 1980) are T. Randall, H. Senou, S.-K. Wu, and two anonymous reviewers.
similar. The period of development within capsules ranged
from 6 to 9 d in C. annulus, the shortest amongst the cy-
praeid species investigated. Veliger size at emergence aver- Literature cited
aged 0.13 ram, similar to that of C. caputserpentis, C. hel-
vola, and C. poraria (Ostergaard 1950). Bandel, K. (1973). Notes on Cypraea cinerea Gmelin and Cyphoma
gibbosum (Linnaeus) from the Caribbean Sea and description of
their spawn. Veliger 15:335-337
Burgett, J. M., CUbit, J. D., Thompson, R. C. (1987). Seasonal
Spawning frequency growth patterns in the tropical littorinid snails Littorina anguli-
fera and Tectarius rnuricatus. Veliger 30:11-23
Tanaka (1980) reported that in capsula time for Cypraea Darling, S. D. (1965). Observations on the growth of Cypraea spadi-
vitellus increased by 75% when seawater temperature was cea. Veliger 8: 14-15
D'Asaro, C. N. (1970). Egg capsules of prosobranch mollusks from
reduced from 26 ~ to 19 ~ The surface seawater temperature south Florida and the Bahamas and notes on spawning in the
varied from 17.8 ~ to 31.4~ at Sesoko, just off Okinawa laboratory. Bull. mar. Sei. 20:414-440
234 M. Katoh: Life history of Cypraea annulus

Frank, P. W. (1969). Growth rates and longevity of some gastropod Perron, F. E. (1986). Life history consequences of differences in
mollusks on the coral reef at Heron Island. Oec~logia 2: developmental mode among gastropods in the genus Conus.
232-250 Bull. mar. Sci. 39:485-497
Griffiths, R. J. (1961 a). Sexual dimorphism in Cypraeidae. Proc. Renaud, M. L. (1971). Aspects of the biology and ecology of Cy-
malac. Soc. Lond. 34:203-206 praea raoneta at Eniwetok Atoll, Marshall Islands. M. S. thesis.
Gfiffiths, R. J. (1961 b). Size and sex in Cypraeidae. Proc. malac. University of Hawaii, Honolulu, Hawaii, USA
Soc. Lond. 34:322-324 Schilder, F. A., Schilder, M. (1961). Sexual differences in cowries.
Kay, E. A. (1960). The functional morphology ofCypraea caputser- Proc malac. Soc. Lond. 34:207-209
pentis L. and an interpretation of the relationships among the Smith, B. D. (1987). Growth rate, distribution and abundance of
Cypraeacea. Int. Revue ges. Hydrobiol. 45:175-196 the introduced topshell Trochus niloticus Linnaeus on Guam,
Kay, E. A. (1985). About the cowries. In: Burgess, C. M. (ed.) Mariana Islands. Bull. mar. Sci. 41:466-474
Cowries of the world. Gordon Verhoef, Cape Town, p, 4-11 Tanaka, Y. (1980). Spawning and development of the cowry, Cy-
Kenny, R. (1977). Growth studies of the tropical intertidal limpet praea (Ponda) vitellus Linnaeus. [in Japanese with English ab-
Acmaea antillarum. Mar. Biol. 39:161-170 stract] Venus, Kyoto 39:117-122
Nakamura, S. (1984). Record of air temperature, surface water Taylor, J. B. (1975). Planktonic prosobranch vellgers of Kaneohe
temperature and chlofinity at Sesoko in 1983. Galaxea 3: p. 105 Bay. Ph.D. dissertation. University of Hawaii, Honolulu,
Natarajan, A. V. (1954). On the breeding habits of the cowry Erro- Hawaii, USA
nea errones (Linnr). Curr. Sci. 23:225-226 Yamada, S. B. (1987). Geographic variation in the growth rates of
Natarajan, A. V. (1957). Studies on the egg masses and larval Littorina littorea and L. saxatilis. Mar. Biol. 96:529-534
development of some prosobranchs from the Gulf of Mannar Yamaguchi, M. (1975). Estimating growth parameters from growth
and the Palk Bay. Proc. Indian Acad. Sci. (Sect. B) 46:170-228 rate data: problems with marine sedentary invertebrates. Oeco-
Okinawa Meteorological Agency (1985). Showa 59 nen no taifu logia 20:321-332
kiroku [in Jap.] [Typhoon records in 1984]. Kajifuchi 13:34-37 Yamaguchi, M. (1977). Shell growth and mortafity rates in the coral
Orr, V. (1959). A bionomic shell study of Monetaria annulus (Gas- reef gastropod Cerithium nodulosum in Pago Bay, Guam, Maria-
tropoda: Cypraeidae) from Zanzibar. Notul. Nat. 313:1-15 na Islands. Mar. Biol. 44:249-263
Ostergaard, J. M. (1950). Spawning and development of some
Hawaiian marine gastropods. Pacif. Sci. 4: 75-115
Perron, F. E. (1983). Growth, fecundity, and mortality of Conus Date of final manuscript acceptance: October 21, 1988.
pennaceus in Hawaii. Ecology 64:53-62 Communicated by J. M. Lawrence, Tampa