Vol. 6; Supplement
Page 56
THE VELIGER
The Responses of Tegula funebralis to Starfishes
and Predatory Snails
(Mollusca : Gastropoda)
JOHN L. YARNALL
Hopkins Marine Station of Stanford University,
Pacific Grove, California
(2 Tables)
the shell away from the point of contact and the snail
INTRODUCTION
either turns away or crawls obliquely away. Contact with
THE RESPONSES of some gastropods to predators are well
the posterior portion of the foot results in the shell being
known (BULLOCK, 1953; CLARK, 1958; FEDER, 1956;
tipped far up over the head and is often accompanied by
SMITH, 1960). This study was designed to investigate the
violent rocking of the shell through an arc of almost 180
responses of a single herbivorous snail, Tegula funebralis
degrees. As before, the snail crawls away at 2 or 3 times
(A. ADAMS, 1854), to a number of predatory and related
normal speed. In the following contact experiments a
forms. They include: the sea stars Pisaster ochraceus
tube foot, excised from a test starfish, was slipped over
(BRANDT, 1835), Pisaster brevispinus (STIMPSON, 1857),
the end of a probe and touched to various soft parts of
Pisaster giganteus (STIMPSON, 1857), Patiria miniata
Tegula. All of the tube feet were of the grasping type,
(BRANDT, 1835), Pycnopodia helianthoides (BRANDT,
taken from the middle 1/3 of a starfish ray.
1835), Leptasterias aequalis (STIMPSON, 1862), Dermas
Contact with the sole of the foot of the carnivorous
terias imbricata (GRUBE, 1857), and the carnivorous
snails Thais emarginata and Acanthina spirata produces
snails Thais emarginata (DESHAYES, 1839), and Acan-
a greater response in Tegula than a similar touch with
thina spirata (BLAINVILLE, 1832). All of these animals
their shell, proboscis, or tentacles. Therefore, in tests with
occur in the rocky intertidal zone, at Mussel Point, Pa¬
these species, small pieces of the foot were applied to
cific Grove, California, with the exception of Pisaster
Tegula in the manner used for the tube feet of sea stars.
brevispinus, which is found in the nearby sandy subtidal
The responses elicited by contact with the foot of
zone. Hereafter the name Tegula will refer to Tegula
Thais emarginata or Acanthina spirata were essentially
funebralis only.
the same as those following contact with starfish tube feet
with one exception. A Tegula stimulated laterally or pos-
CONTACT EXPERIMENTS
teriorly first twists its shell away from the area of stimula¬
tion, but instead of crawling away it raises its head and
FEDER, (1956) and BULLOCK, (1953) indicate that the
foot and turns toward the point of contact, crawling up
tube feet of starfishes, when they are placed in contact
onto the predator tissue. Placing a shell of the carnivore
with a snail, elicit a greater response from gastropods than
in the path of the Tegula causes it to climb rapidly onte
do any other portions of the starfish body. The responses
the shell.
of Tegula to the tube feet of most of the starfishes tested
The responses enumerated above were not merely re-
are essentially the same as those described by FEDER,
actions to any foreign object. Contact with a clean bare
(1956 pp 143-145) for Pisaster ochraceus and Tegula. Ii
probe only causes a Tegula to retract that part of its body
a Tegula is stimulated in the head region the snail rears
which has been touched and to clamp its shell down
back, raising its head and the anterior portion of its foot.
tightly against the substrate.
This is followed by a turn of approximately 90 degrees
Each predator was tested against 50 Tegulas, 25 of
and the snail crawls away rapidly. Lateral stimulation of
which were stimulated first with the control probe and
the foot and epipodium causes a tipping or twisting of
Page 57
Vol. 6; Supplement
THE VELIGER
sea water, and 25 Tegulas, ranging in basal shell diam¬
then the predator tissue. The order of applying the two
eter from 5 mm to 30 mm, were aligned on the periphery
stimuli was reversed for the other 25. The Tegulas tested
of the bottom. Five minutes later the number of snails
ranged in size from 5 mm to 30 mm in maximum basal
diameter of the shell. To avoid any possible habituation to
with their heads out of water was recorded, and the same
the various stimuli, each T’egula was taken from the shore,
snails were again placed along the bottom of the pan.
A predator was placed in the center of the pan and the
used once, and then returned to the beach.
number of snails with their heads out of water at the
In Table 1 responses to contact with both predator
end of 5 minutes was again noted. The snails were used
tissue and the control (probe) are indicated. All responses
in only one experiment (including control) and each ex¬
were typical of the descriptions above but varied in inten-
periment was repeated 5 times. When necessary the pred¬
sity. A strong response consists of an immediate reaction
ator was placed in a plastic bag to prevent contact with
following a single stimulus. Moderate responses are those
the Tegulas. Because of the small size of a few of the pred-
in which the reaction was slower and more than one
application of the stimulus was required. Where no re¬
ators, several were placed in a cage and used at one time.
sponse is recorded the animal completely ignored the
Table 2
stimulus. The test animals are listed in the table in order
of strength of response elicited, the strongest first.
The Responses of Tegula funebralis to Diffusible
Substances from Predators
DIFFUSION EXPERIMENT
Predator
Trial
PHYSICAL contact between Tegula and predatory star-
fishes is not always necessary to produce a response on
Pycnopodia heli-
19/4 4/0 17/1 19/0 13/0
the part of the mollusk (Bullock, 1953; Feder, 1956).
anthoides
To further test the hypothesis that substances diffusing
Pisaster giganteus
6/2 19/3 6/2 9/0
11/1
from a predator can cause a reaction in T’egula the fol¬
17/3
8/0 7/3 5/0
Pisaster ochraceus
lowing series of experiments was performed. A clean
Leptasterias aequalis
4/1 11/1 8/1
10/1
plastic dishpan was filled to a depth of 6 cm with fresh
Pisaster brevispinus
3/0 6/0 5/0 13/0 5/0
Table 1
Acanthina spirata
2/1 3/0 1/2
0/0 4/1 2/4
Thais emarginata
0/0
The Responses of Tegula funebralis to Contact with
0/0 2/0 1/0 0/1 1/1
Patiria miniata
Predator Tissue and with a Clean Probe
Dermasterias
1/0 1/1 0/0 1/1 0/1
Response of Tegula funebralis
Predator
imbricata
to contact with:
Experimental situation/Control situation. Figures repre¬
Predator
Clean
sent the number of Tegula funebralis with heads out of
water at the end of five minutes; N = 25 for each trial.
Tissue
Probe
SMWO
SMWO
Animals used in this manner were Leptasterias aequalis
Pisaster giganteus
6 82 12
(16), Thais emarginata (26), Acanthina spirata (21).
Pisaster ochraceus
88 10
16 70 14
In all other cases a single predator was used. The results
Acanthina spirata
6 82 12
84 12
of the diffusion experiments are indicated in Table 2. The
Pisaster brevispinus
10 84 6
80 12
test animals are listed in order of number of Tegulas re¬
26 70
Thais emarginata
76 20
sponding to them, greatest number first.
Pycnopodia heli-
16 76
64 32
anthoides
DISCUSSION
44 38 16
Leptasterias aequalis
12 80 8
The responses tabulated in Table 1 indicate that Tegula
0 14 86
Dermasterias
6 84 10
responds differently to the predators and the non-pred-
imbricata
ators used in these tests. Patiria miniata is an omnivorous
Patiria miniata
O0 892
6 88 6 0
scavenger and herbivore and Dermasterias imbricata is
Figures are percentages of animals tested which gave the
thought to be a scavenger on dead animal matter, while
response indicated. N = 50, S = Strong response,
the remainder of the test species are active carnivores,
Moderate response, W = Weak response, and O — No
all of which have been observed eating Tegula either in
response
the laboratory, in the field, or both. The survival ad¬
Vol. 6; Supplement
Page 58
THE VELIGER
SUMMARI
vantages of escape behavior have been pointed out by
Feder (1959), in his discussion of the food habits of
THE REACTIONS of Tegula funebralis were tested to a
Pisaster ochraceus. He finds that although Tegula is rela-
number of starfishes and carnivorous snails. The responses
tively abundant it is not eaten as frequently as its numbers
vary according to the type of animal used as a source of
might suggest, and that this is due, in part, to the effective
the stimulus. Tegula flees from the contact or presence of
escape mechanisms it has developed. Clark (1958) has
predatory starfishes, ignores non-predaceous ones, and
been able to induce responses in herbivorous gastropods
attempts to escape from or crawl upon the shell of the
by stimulating them with carnivorous ones. The reactions
carnivorous snails used in these tests. Strong escape re¬
are described as similar to those mentioned by Bullock
sponses were elicited on contact with predatory starfishes
(1953). Tegula’s response to 2 carnivorous snails, how¬
such as Pisaster ochraceus, P brevispinus, P giganteus,
cver, has been to go toward the carnivores and attempt
Pycnopodia helianthoides, Leptasterias aequalis and the
to crawl up over them. This, too, appears to have survival
carnivorous snails Thais emarginata and Acanthina spira¬
value.
ta, but not to the non-predatory sea stars Patiria miniata
That the responses are stimulated by a chemical signal
s indicated by the difference in type of response elicited
and Dermasterias imbricata. Escape reactions are also
elicited by substances diffusing from the 5 predaceous sea
by contact with predator tissue and clean probes. The
stars listed above. No similar response is caused by the
substance appears to be diffusible in the case of starfishes
other test animals.
and non-diffusible in the case of snails (Table 2).
While Leptasterias aequalis is too small to eat the larger
l'égula specimens it can certainly eat the smaller ones,
LITERATURE CITED
and the reactions of the large Tegulas may be a retention
BULLOCK, THEODORE HOLMES
of a response adaptive in earlier life or to starfish in gen-
Predator recognition and escape responses of some inter¬
1953.
eral. The one T’egula which gave no response to L. aequa-
tidal gastropods in the presence of starfish. Behaviour
lis and 6 of those which gave a weak response were 20 mm
5 (2): 130- 140
in basal shell diameter or larger.
CLARK, W. C.
From the small number of predator species tested it is
Escape responses of herbivorous gastropods. Nature
1958.
difficult to predict any correlation between sympatry of
181: 137 -138
the predators and Tegula, and the responses of Tegula
FEDER, H. M.
to the predators. However, Pisaster brevispinus must sel¬
Natural history studies on the starfish Pisaster ochra¬
1956.
dom, if ever, be encountered by Tégula yet this starfish
ceus, in the Monterey Bay area. unpubl. Ph. D. Thesis,
elicits a strong escape reaction. It may be that there are
Stanford Univ.; Stanford, Calif.
substances peculiar to the physiology of predatory asteroids
The food of the starfish. Pisaster ochraceus, along the
1959.
and gastropods in general which Tegula can recognize
California coast. Ecology 40 (4) : 721 -724
If this is so then little, if any, correlation between response
SMITH, DEBOYD L.
and sympatry of predator and Tegula is to be expected,
1960. Stimulus-response relationship between certain mollusks
but rather a correlation between feeding habit and escape
and starfish. unpubl. student report, Hopkins Marine Sta.,
reaction.
Stanford Univ., Calif.
Page 59
Vol. 6; Supplement
THE VELIGER
Shell Growth and Repair in the Gastropod Tegula funebralis
(Mollusca: Gastropoda)
MARGARET CAROLINE PEPPARD
Hopkins Marine Station of Stanford University,
Pacific Grove, California
(3 Text figures; 2 Tables)
chlamydospores (see Fig. 3) which differ from those on
SHELLS OF Tegula funebralis (A. ADAMS, 1854) inhabit¬
the species raised by BONAR, and also from those found by
ing the intertidal areas of Mussel Point, Pacific Grove,
JOHNSON (1962) in a fungus growing on smooth jingle
California, are rarely found to have more than four
shells (Anomia simplex D’ORBIGNY) from Pivers Island
whorls, irrespective of the size of the snail, due to heavy
beach, North Carolina
erosion of the upper parts. Questioning the nature of
Normal shell growth in Tegula funebralis was measured
repair of erosion damage led to a consideration of the
for a fifteen-day period (May 14-29, 1963) on individuals
more general question of shell repair in T. funebralis.
ranging 13.0-27.5 mm in greatest basal diameter. Meas
FRETTER & GRAHAM (1962) discuss shell formation in
urements were made with an ocular micrometer of growth
prosobranch molluscs, but little is understood of shell re
increments on the outer lip of the aperture, secreted on
pair mechanisms
Tegula funebralis lives in what is essentially a tapered
tube, closed at the small end. This is clearly seen in Figs
Explanation of abbreviations used in the figures:
1 and 2. Macroscopically, there are three layers in the
a - shell aperture; an - anus; cm - columellar muscle
shell. The thin, transparent periostracum on Mussel Point
ct - ctenidium; e - eye; f- foot; g- gonad; h - heart;
specimens is present only on the body whorl near the
ht - head tentacle; k - kidney; me- mantle cavity;
shell aperture, if at all. Underlying the periostracum is
op - operculum; os - osphradium; r- rectum; s- shell;
a black prismatic layer. These two layers are secreted
sc - spiral caecum; st - stomach.
only by the mantle margin. Innermost is a thick nacreous
layer, white over most areas, but sometimes yellow or
greenish in the upper whorls. Slides of decalcified shells
mo
embedded in paraffin show the laminar character of the
nacreous matrix.

Most of the specimens of Tegula funebralis from Mussel
M
Point have shells which are conspicuously eroded. Al¬
though some of the erosion appears to be due to the
radular action of predaceous snails, boring of bryozoans


and polychaetes, or mechanical wear, all save a minority
of T. funebralis (individuals measuring 5 mm or less at

the greatest basal diameter) are pitted over most of the


eroded surface. Under 30x magnification, this damage
closely resembles that caused by a fungus described as in¬

.
festing shells of marine animals by BONAR (1936). At
tempts were made to culture the fungus on T. funebralis
on a medium of 100 ml sea water, 1 gm CaCO, 1 ml 1 M
NaNOs, 1 ml 1 M KH-PO., 1.5 gm agar, 1 gm humus,
Figure 1: Ventral view of Tegula funebralis, 8 mm in
5 gm T. funebralis shell, finely ground, 0.1% glucose,
basal diameter; decalcified, cleared in cedarwood oil.
and 0.01% yeast extract. The fungus in culture shows
and with black prismatic layer removed.
Page 60
Vol. 6; Supplement
THE VELIGER
Table 1
Growth Studies on the Shell of Tegula funebralis
Addition to Shell at Aperture on Successive Days
Snail Greatest
Average
basal
growth
(mm)
diam. (mm)
per day
13.0
.090
.006
060
.014
120
210
16.0
.030
060
17.0
030
060
090
.006
17.0
030
.004
060
18.0
.002
18.0
030
060
.004
19.0
20.0
090
.008
090
20.5
120
.008
1.0
165
011
.033
165
011
.060
.090
.006
.090
120
150
.010
030
060
090
.006
030
.060
.004
23.0
.060
030
24.0
.090
.006
24.0
.060
24.0
090
.006
060
24.5
.090
120
.008
25.0
015
120
.008
030
.008
25.0
.090
25.5
030
.002
132
165
.011
.060
007
0
060 —
120
.008
Legend:
no change since last observation
no observation
X dead
in various ways, inflicting different types of shell dam-
top of a baseline of fingernail polish painted on the edge
of the aperture at the beginning of the study. Results are
age, as indicated in Table 2. Five individuals were oper-
shown in Table 1. The average overall addition to shell
ated in each way. The holes (windows) made in the shell
aperture was six microns per day, but growth occurred in
back of the aperture were ground on an emery wheel,
spurts, not evenly each day. Total growth over the fifteen-
care being taken to keep the shell wet and cool, and the
day period did not measurably affect the greatest basal
internal tissues intact. Table 2 gives the average change
diameter of the shells.
in each group on successive days. The range of variation
In order to assess the ability of Tegula funebralis to re¬
within each group was not so great as to make the aver-
age irrelevant. In every case of damage to the shell
pair damage incurred to the shell, snails were operated on
Page 61
Vol. 6; Supplement
THE VELIGER
Table 2
Repair of Shell Damage in Tegula funebralis
Repair on Successive Days Äfter Operation
Type of Operation
(mm Added to Shell at Aperture)
control (no opera¬
165
tion; normal growth
at aperture lip
recorded)
mantle margin slit
2mm
notch
filled
notch
2.6 mm notch filed
O66mm
240mm
388mm
479mm .677mm
in edge of shell
of notch
aperture
notch
filled
notch
notch
notch
filled
filled
filled
filled
window over
Caco,
2 CaCO.
O
visceral hump
layers
window over heart
M CaCO,
and kidney area
window over mantle
198
353 397
cavity
added
to hole
edge
shell cracked
M
CacO,
white
(with a vise)
nacreous
secretion
over
crack (xx)
shell broken at
187
221
386
354
aperture (with
pliers)
shell aperture
333
353
397—
583
ground off
G
no change since last observation
M soft, membranous layer secreted over opening
no observation
CaCO, dead
T just visible trace of nacreous layers secreted
X calcium carbonate embedded in soft laver
Vol. 6; Supplement
Page 62
THE VELIGER
me
Snails with openings over the visceral hump first se-

creted a soft, membranous layer across the inside of the

hole; this later became impregnated with calcium carbo¬
nate. Successive layers, similar in appearance, were built
up beneath the first layer, which bulged through the
opening. After thirty days (April 30-May 29, 1963), one
specimen had plugged the shell window with a hard patch
of white material, apparently calcium carbonate em¬

bedded in an organic matrix. The patch protruded
through the opening like a bubble, and was translucent
at the periphery, opaque in the center portion. Of three
females and two males, with windows cut over the vis-
ceral hump, the females began repair sooner than the
males. None of the snails with windows over the visceral
hump died, although the gonad was frequently ruptured.
On the other hand, animals with the shell damaged by
grinding a hole over the region of the heart and kidney
Figure 2: Dorsal view of Tegula funebralis, same
died in all cases except one. Death was due not to the
individual as shown in Figure 1.
operation, but to the later rupture of the kidney or peri-
aperture, growth of the damaged part proceeded faster
cardial sac against the sharp edge of the opening pro¬
than the growth at apertures of undamaged controls. All
duced by the operation. One specimen which lived an
such operations on the apertures were repaired by the
entire month with this operation failed to successfully
folds at the border of the mantle. The same was the case
repair the damage, for each time the soft membranous
with the windows over mantle cavities. New shell material
layer covering the hole became embedded with calcium
included a black prismatic layer.
carbonate, it was sloughed off through the opening.
When the mantle margin was slit in an otherwise un
In the "windowed" animals, even where the holes
damaged specimen, within two days a notch appeared
penetrated yellow and green layers, I observed no secre-
in the shell aperture at the point apposed to the incision
tion of yellow or green material by the mantle covering
It is not clear whether the notch was due only to lack
the body, nor is it secreted by the mantle margin. Se¬
of growth, or in part due to active resorption of shell at
cretions by other than the mantle margin were always
the point, but within six days the notch was repaired.
either transparent membranous layers or white inorganic
material. However, natural repair does show yellow or
green material, particularly in eroded areas at the shell
apex. Perhaps the inner layers of nacreous material are
dyed by pigments secreted by the visceral hump, specif-
ically either the digestive gland or the gonad (see Mc-
GEE, 1964).
Cracked shells were bound firmly together in a solid
unit within five days by a calcium carbonate-embedded
membrane on the inner surface. Additional white nacre
ous material was laid over the outer surface of the crack
within eight days where the break passed through the
underside of the body whorl adjacent to the shell aperture.
JMMARY
1. Shell erosion is caused by the activities of several ani-
mals (bryozoans and polychaetes), by mechanical wear,

and by a fungus, which was cultured on agar plates.
2. Normal shell growth, recorded over a period of fifteen
days in twenty-eight animals, was intermittent, but
averaged six microns per day added to the outer lip
Figure 3: Fungus found on Tegula funebralis shell;
of the aperture.
part of mycelium with chlamydospores.
Vol. 6; Supplement
Page 63
THE VELIGER
FRETTER, VERA, & ALASTAIR GRAHAM
3. Repairs to shells damaged mechanically, by filing
1962. British prosobranch molluscs; their functional anatomy
the aperture, grinding holes in the body and upper
and ecology. London, Ray Soc.; xvi + 755 pp.; 317 figs.
whorls, and by cracking in a vise are described.
JOHNSON, T. W., Jr. & W. A. ANDERSON
1962. A fungus in Anomia simplex shell. Journ. Elisha Mit¬
LITERATURE CITED
chell Sci. Soc. 78: 43 -47
BONAR, L.
MCGEE, PATRICIA
1936. An unusual ascomycete in the shells of marine animals.
1964. A new pigment from Tegula funebralis (Mollusca: Gast¬
Univ. Calif. Publ. Bot. 19: 187 -194
ropoda).
The Veliger 6; Supplement: 25 - 27; 1 text fig.
The Dispersal of Young of the Commensal Gastropod
Crepidula adunca from its Host, Tegula funebralis
DEBORAH A. PUTNAM
Hopkins Marine Station of Stanford University
Pacific Grove, California
(4 Text figures)
INTRODUCTION
HATCHING
Crepidula adunca breeds the year round (MORITz, 1938
Crepidula adunca SowERBy, 1825 is a protandric marine
prosobranch commonly found on the shells of Tegula
The animals used were gathered from Mussel Point,
Pacific Grove, California. Tegula funebralis with the
funebralis (A. ADAMS, 1854), both when the latter is
brooding Crepidula females were kept in glass finger
occupied by the snail and when it is occupied by Pagurus
spp. MORITZ (1938) gives the range of C. adunca as
bowls at 12 to 18° C. Young when hatched were kept
being similar to that of T. funebralis: from Vancouver
similarly. All young used in all experiments were hatched
British Columbia, to the tip of Lower California. CONK¬
without human assistance, both to avoid harming the
young through attempts to liberate them artificially
LIN (1897) has followed the cell lineage of C. fornicata
and C. plana, and MoRIrz (1938, 1939) has treated the
and to establish their age, as the period of development
anatomy and organogenesis of C. adunca.
to hatching is not known.
In the four cases where hatching was observed, young
Crepidula adunca undergoes a very direct develop-
Crepidula adunca were released between 8:30 and 10:30
ment from large, yolky eggs which are brooded by the
female. The hatching young crawl out of the egg cases
a. m. The egg cases are attached by individual stalks to
as juveniles which are similar to adults. At hatching there
one spot on the Tegula funebralis shell, immediately
may be from 150 to 200 young released. Although no
ventral and posterior to the head and anterior to the foot
pelagic stage is present, the adult population of C. adunca
of the female C. adunca. Normally, the female's shel
is quite well dispersed over the Tegula funebralis popu¬
is lifted no more than 0.5 mm above the substrate, only
lation near the Hopkins Marine Station, Pacific Grove,
enough to allow water to flow through the mantle cavity
for filter-feeding and respiration. During hatching, how¬
California. The number of adult C. adunca per T. funeb¬
ralis shell is relatively low (eight was the maximum
ever, the female intermittently lifts her shell 1 to 3 mm
above the substrate, for periods which varied from 3.5
number seen) as compared to the large number of young
seconds to about 4 minutes. Then with a forward and
per brood. Clearly, the young become dispersed to new
downward motion of her head over the egg cases, the
hosts without benefit of a pelagic stage. How this is
female pushes out those of her young which are loose
accomplished is the subject of the present investigation.