Deborah S. Yokoe
INTRODUCTION
Crepidula adunca (Sowerby, 1825), commonly known as
the slipper shell, is a protandric marine prosobranch
commonly found intertidally on the shells of the black
turban snail Tegula funebralis (A. Adams, 1854). Its
range extends from Vancouver, British Columbia, to the
tip of Lower California.
Crepidula adunca females brood a mass of yolky eggs
until developed and will physically push the young into
the surrounding water (Putnam, 1964). The young lack
sexual organs and after a growth period develop a penis
and enter the male phase of their life cycle. At some
point, dependent partly upon environmental factors, the
Crepidula enter the female stage of their life cycle
(Coe, 1936). The male is typically found oriented on the
female shell which in turn is oriented on the T. funebralis
shell (Coe, 1953).
Crepidula adunca reportedly use a radula for rasping
algal films from rocks when young and switch to a filter-
feeding system as they mature into adults (Coe, 1948;
Abbott and Haderlie, 1980). The results of this investi¬
gation suggest that in terms of feeding behavior, both
young and adults may be more labile than previously believed.
Newborn Crepidula adunca have a mean length of about
1.18 mm and are very similar to the adults in appearance.
Essentially nothing was known about the period of the
Crepidula life cycle between the time of dispersal and the
time of attachment to Tegula. Although newborn Crepidula
are about 1 mm in length, previous investigators (Putnam,
Deborah S. Yokoe
1964) were unable to find Crepidula adunca smaller than
3.8 mm in length in the field. This investigation was
focused towards solving the mystery of the habitat of the
young after dispersal. The results obtained suggest that
young Crepidula adunca attach to small gastropod shells
in sandy, shell-fragmented areas neighboring the rocky
areas where the adults are found on Tegula funebralis.
MATERIALS AND METHODS
I. Comparison of young and adults
A Crepidula hatchery was set up by placing Tegula
with male-female Crepidula pairs in aquaria and collecting
the young as they were dispersed. The first phase of this
investigation involved comparison of the behavior and
desiccation tolerance of young and adult Crepidula through
experimentation in the laboratory. The motility of young
was compared to that of adult males and females by measuring
the distances from the point of origin of individual
Crepidula over intervals of five minutes in a large glass
dish. Vulnerability to desiccation was tested by removing
the animals from water, placing them on a glass surface,
and examining them periodically for response to probing.
Death was defined operationally as failure to respond to
probing stimuli after reimmersion in seawater for 30 minutes.
The feeding behavior of the young was compared to
that of the adult by observing radular rasping action or
filter-feeding. To test for radular feeding, a Crepidula
was placed on a diatom-covered slide turned upside-down
into a shallow dish of water and observed under a dissecting
microscope for scraping of diatoms by the radula. In order
Deborah S. Yokoe
to determine whether an animal was filter-feeding, it was
placed on a clean microscope slide, placed upside-down
in a shallow dish of water with a few drops of graphite
solution, and examined under the dissecting microscope
for the appearance of a graphite-blackened mucus string
travelling to the mouth up the ciliated food groove located
on the right neck lappet.
An artificial microhabitat was set up in the laboratory
by placing a layer of sand covered by shell fragments
and rocks in a large glass dish along with gastropods and
Pagurus in gastropod shells ranging from 2 mm to 20 mm in
length. 20 newborn Crepidula were added, and the micro-
habitat was left undisturbed for a week.
II. Field Studies
Areas of high adult Crepidula density and the surrounding
regions of the intertidal were examined for the presence
of young Crepidula. Distribution of Crepidula on hosts
of adult Tegula funebralis on rock faces was surveyed by
collecting each sample within a haphazardly placed quadrant
of area of 1 m2. Distribution of Crepidula on host gas-
tropod shells of sandy bottoms was surveyed by collecting
samples of approximately equal volumes from the bottom in
a metal scooper.
III. Attraction of Crepidula to T. funebralis
Preference tests were performed between live T. fune¬
bralis and empty T. funebralis shells, between T. funebralis
funebralis shells, and between T. fune-
and Pagurus in T.
bralis shells and T. funebralis which have had their outer
black layer sanded off. These tests involved placing
Deborah S. Yokoe
a male Crepidula in the center of a glass dish with, for
example, a live Tegula and a Tegula shell, at opposite
sides of the dish and examining the attachment of the male
Crepidula after 24 hours.
Experiments to examine the possible protection from
predation by attachment of Crepidula to a Tegula shell
were performed by placing 5 male Crepidula, 5 T. funebralis,
and 5 Pagurus in T. funebralis shells together in a glass
dish and observing survival rate of Crepidula over time.
ESULT
The motility experiments (Fig. 1) show that the young, which
although in body length are an average of 10 times smaller
than the females and 7 times smaller than the males, ex-
hibit greater movement over time than either the males or
females. The young show an average distance moved over
30 minutes of 3.18 cm, the adult males show an average
distance moved of 2.16 cm, and the adult females show an
average distance moved of 2.04 cm.
Desiccation experiments showed the young to be much
more vulnerable to desiccation than the adults. When placed
out of water, the young die within 15 to 20 minutes while
the adults are able to survive for several hours.
Observation of feeding behavior of the newborn indicate
that Crepidula adunca are born not only with the ability
to rasp but also with the capacity to filter-feed. Although
the food pouch does not develop until after the young adult
stage (Moritz, 1939), a mucus string travelling up the
Debor
ah S. Yok
food groove to the mouth was clearly observed in the newborn.
Similarly, although adults reportedly lose their ability
to feed by rasping, a definite scraping by the radula
of diatoms off of the slides was observed not only by the
young but also by both adult males and females.
After an interval of a week, the microhabitat which
had been constructed to resemble the sandy, shell-fragmented
habitat of the young, resulted in a clustering of newborn
Crepidula on the smallest gastropod shells available.
19 out of 20 were found on shells smaller than 8 mm in
length and no Crepidula were found attached to adult T
funebralis.
Examination of rock faces and crevices where adult
Crepidula are abundant yielded no Crepidula smaller than
4 mm in length. Examination of nearby sandy, shell-frag-
mented areas and sandy holdfasts of algae and Phyllospadix
revealed a number of small gastropod shells and Pagurus
in small gastropod shells with Crepidula attached which
ranged down to the 1 mm size of newborn Crepidula (Fig. 2). The
results of the distribution survey in the lower, sandy,
shell-fragmented habitats are shown in Fig. 3, in which
the number of host shells, host shells with Crepidula, and
host shells with Crepidula of 1 mm in length for each host
shell size class are shown. The abundance of small gastropod
shells and the clustering of the newly born Crepidula on
the smallest gastropod shells are apparent. The average
size of Crepidula found is 2.00 mm with a standard error of
.18. The average size of host shells with 1 mm Crepidula
attached is 3.90 mm with a standard error of .32. The average
Deborah S. Yokoe
size of shells with Crepidula attached is 6.67 mm with a
standard error of .61. The average size of all potential
host shells is 7.02 mm with a standard error of .27.
18.1% of all potential host shells had Crepidula attached.
In contrast, the distribution of shells in the rock face
habitat shows an abundance of large host shells and a com¬
plete absence of Crepidula of 1 mm (Fig. 4). Average
size of Crepidula found is 8.25 mm with a standard error
of .52. The average size of all potential host shells
is 15.74 mm with a standard error of .17. The average size
of host shells with Crepidula attached is 17.18 mm with a
standard error of .32. 13.2% of all potential host shells
had Crepidula attached. The data indicate that there is
a clustering of small Crepidula and gastropod shells and
a correspondence between size of Crepidula and size of
host shell in the sandy habitat which are lacking in the
rock face habitat.
Fig. 5 shows the relationship between size of Crepidula
and size of host shell found in the sandy habitats. A
least squares linear regression was performed and yielded
the line y-.19 +.28x which appears on the graph. A Pearson
R correlation coefficient of R=.81 was obtained, indicating
a strong correlation between Crepidula and host shell
sizes. Also apparent is an increasing variability in
Crepidula sizes found on host shells with an increase in
host shell size. In contrast, size of Crepidula versus
size of host shell in the rocky habitats (Fig. 6) show
essentially no correlation, a large range of Crepidula
sizes found on all host shell sizes present. Also of note
Deborah S. Yokoe
is the absence of small host shells and Crepidula smaller
than 4 mm.
The results of the preference tests performed with
adult Crepidula over an interval of 24 hours indicate
that adult Crepidula showed no preference between T.
funebralis and empty T. funebralis shells (P».05), no
preference between T. funebralis and Pagurus in T. fune-
bralis shells (P).05), and no preference between T. fune¬
alis shells and T. funebralis shells which have had their
outer layers sanded off (P).05).
Predation experiments resulted in a 100% survival rate
of Crepidula. Within about 15 minutes all Crepidula had
attached to either a T. funebralis or Pagurus in T. fune-
bralis shell. Even after 2 weeks of starvation, the Pagurus
made no attempt to remove Crepidula from Tegula shells.

DISCUSSTON
Field studies indicate that young Crepidula adunca
are found in sandy, shell-fragmented areas and among the
sandy holdfasts of algae and Phyllospadix neighboring
the rocks of the adults.They are on small gastropod shells
including juvenile T. funebralis and small gastropod
shells occupied by Pagurus. This habitat seems to fit in
well with the information known about newborn Crepidula.
By attaching to organisms which prefer sandy, lower habitats
almost constantly immersed in water, the young Crepidula
are able to avoid conditions conducive to desiccation
which the adult Crepidula on T. funebralis, often found
(Wara and Wright, 1963), are able to with-
out of water
Deborah S.
Yokoe
stand. The shell fragments and blades of algae characteris¬
tic of the habitat of the young may provide protection
from strong water currents which might tend to tear the
young Crepidula away from the host shell. Putnam (1964)
found that newly dispersed young, because of their inability
to free swim, will fall off the host shell and sink. This
characteristic of the young would provide an effortless
means of transportation between the rock face habitat
of the adults and the sandy bottom habitat where the young
are found. The ability to both rasp and filter-feed indi-
cated in laboratory observations would grant the young
more flexibility in habitat choice.
The strong positive correlation between size of Crepi-
dula and size of host shell in the sandy habitat seems to
suggest that very small Crepidula will attach to a small
gastropod shell until it outgrows it, at which point it
will move on to a bigger host shell. At some point in its
life cycle, however, Crepidula seem to develop a strong
attraction for the Tegula funebralis and female Crepidula
shells and will settle down on one host for long periods
of time. This prolonged attachment of male and female
Crepidula of various ages would result in the wide range
of Crepidula sizes found on the adult T. funebralis shells
of the rocky habitats. The relatively high motility of
the young fits in well with the possibly higher rate of
host exchange of the young indicated in the laboratory.
The lack of attraction towards adult T. funebralis or
Deborah S. Yokoe
10
Crepidula adunca in the young and strong attraction of the
adult observed by Putnam (1964) would also fit in well
with the transition from sandy habitats where Crepidula
are found attached to a variety of small shells to rocky
habitats where T. funebralis are found almost exclusively.
The attachment behavior of the young in the artificial
microhabitat also confirms the preference of newborn
Crepidula for small gastropod shells.
The predation experiments suggest that attachment of
Crepidula to Tegula shells may serve as a means of protec-
tion from Pagurus predation.
The preference experiments were designed to explore
the question of what actually attracts the adult Crepidula
adunca to the host T. funebralis shell. The lack of preference
between live Tegula and empty Tegula shells and between
Tegula and Pagurus in Tegula shells both seem to imply
that the main attracting agent is not the live T. funebralis
animal. The lack of preference between scraped and unscraped
T. funebralis shells indicates that the outer material
and texture of the shell does not serve as the main attrac¬
tant. The shape of the Tegula shell may be the factor which
triggers the attachment behavior of the Crepidula. Rolfes
and Turken (1979) found that Crepidula adunca exhibited
a definite host species preference for T. brunnea and T.
funebralis over T. montereyi which corresponds to a gradient
in shell roundedness. This finding suggests that Crepidula
may use host shell shape as a criterion for attachment.
If this is the case, an increased sensitivity to host shell
Deborah S. Yokoe
11
shape may be the cause of attraction of Crepidula for T.
funebralis and together with the selection of larger host
shells may result in the change of habitat to the rock
faces where Tegula are abundant.
Thus, the results of motility, desiccation, and micro-
habitat experiments as well as observations of feeding and
dispersal behavior harmonize well with the discovery of the
sandy, shell fragment habitats of young Crepidula adunca
below the neighboring rocky habitats of the adults and with
the observation that the young prefer small gastropod shells
as their hosts.
A marked difference in the behavior of the young in
subtidal populations may exist. Young Crepidula adunca
are reported to have been found on adult Tegula species
common to the subtidal region. This may possibly be due
to the difference in habitat conditions, such as the lessened
threat of desiccation in the subtidal areas, or possibly
even due to genetic differences between intertidal and
subtidal populations of Crepidula adunca. Although the
question of where intertidal Crepidula adunca go after
dispersal has been partially answered by this investigation,
a whole range of questions yet to be answered have arisen.
SUMMARY
The young of intertidal Crepidula adunca are dispersed
from the female and sink down into sandy, shell-fragmented,
lower habitats where they attach onto small gastropod
shells. As they outgrow the host shell, they move onto
Deborah S. Yokoe
larger gastropod shells, producing a strong correlation
between size of Crepidula and size of host shell. At some
point in their life cycle, the Crepidula experience a strong
attraction towards Tegula funebralis shells which does
not involve the actual animal or the shell surface material
or texture but rather possibly an increased sensitivity
and/or attraction towards Tegula shell shape. At this point
the Crepidula attach to adult T. funebralis which prefer
rock faces and crevices. It is in these rocky habitats that
the adult Crepidula are found most abundantly in the inter-
tidal region.
Deborah S. Yokoe
TEE
ACKNOWLEDGEMENT
The results of this investigation are due in large
part to the guidance and support of Charles Baxter.
Thanks is also due to Dr. Donald P. Abbott for background
information concerning Crepidula adunca, to James Watanabe
for use of equipment and subtidal expertise, and to Mike
Rothman, Richard Peters, and Peter Gerbino for invaluable
assistance during the quarter.
Deborah S. Yokoe
LITERATURE CITED
Abbott, Donald P. and Haderlie, Eugene C. 1980. Prosobranchia:
Marine Snails, Chapter 13 in Morris, Abbott, and Haderlie
Intertidal Invertebrates of California. Stanford University
Press, Stanford CA, 928 pp.
Coe, Wesley R. 1936. Sexual phases in Crepidula. J. Exp.
Zöól., Philadelphia. 72 (3): 455-476.
Coe, Wesley R. 1948. Nutrition and sexuality in protandric
gastropods of the genus Crepidula. Biological Bulletin.
94 (2): 158-160.
Moritz, C.E. 1938. The anatomy of the gastropod Crepidula
adunca Sowerby. University of California Publications
in Zöölogy. 43 (5): 83-92.
Putnam, Deborah A. 1964. The dispersal of young of the
commensal gastropod Crepidula adunca from its host
Tegula funebralis. The Veliger 6 (Supplement): 63-66.
Rolfes, Richard H. and Turken, David S. 1979. Factors
affecting the distribution of Crepidula adunca on
the host genus Tegula. Unpublished Hopkins Marine
Station paper.
Deborah
Yokoe
15
Wara, William M. and Wright, Benjamin B. 1964. The distri-
bution and movement of Tegula funebralis in the intertidal
egion of Monterey Bay, California. The Veliger 6
(Supplement): 30-37.
FIGURE CAPTIONS
Figure 1: Comparison of the distance covered by young, adult males,
and adult females over a 30 minute period.
Figure 2: Comparison of the habitat locations of young and adult
Crepidula adunca.
Figure 3: Number of shells, number of shells with Crepidula
attached, and number of shells with Crepidula of 1 mm attached
for each host shell size class in the sandy habitats of the
young.
Figure 4: Number of shells and number of shells with Crepidula
attached for each host shell size class in the rocky habitats
of the adults.
Figure 5: Relationship between size of Crepidula and size of host
shell found in sandy habitats. Least squares linear regression
line is shown.
Figure 6: Relationship between size of Crepidula and size of host
shell found in rocky habitats.
Figure 7: Results of preference tests performed with male Crepidula.
Young

0

—

10
Adult Males
3

6 2
a1

—
taaa-
10
Adult Females
2


15 20 25 30
10
TIME (min)
2
ADULT HABITAT
rock face


water
holdfast

shell fragments
sand
HABITAT OF YOUNG
80
72
64
56
48
5 32
2 24
16
shells,
Sshells with Crepidula
shells with Crep. of Imm



2 4 6 8 10 12 14 16 18 20
HOST SHELL SIZE (mm)
80
72
64
56
48
32
224
16
shells
shells with Crepidula
.. .
.



2 4 6 8 10 12 14 16 18 20 22
HOST SHELL SIZE (mm)
20
18
14
412
o
u 8
6

3 . .

223.
zer:.


2 4 6 8 10 12 14 16 18 20
SIZE OF HOST SHELL (mm)
20
19
18
17
14
13
E 12
o.
8
. ** *
. 3
3 . 3
3 . 3 . .
3
3 3 . .
e
. . 3
*
3 .
3 .
2 4 6 8 10 12 14 16 18 20 22
SIZE OF HOST SHELL (mm)