Tegula and Benthic Predators
ABSTRACT
This study investigates the chemoreceptive abilities and escape
responses of Tegula brunnea, T.montereyi, and T.pulligo to common
predators. The predators studied were the sea stars Pisaster
giganteus and Pycnopodia helianthoides, and the crab Cancer
antennarius. T.brunnea and T.pulligo could both detect Cancer from
waterborne olfactory cues. Furthermore, all three Tegula species
took a significantly longer time to emerge from their shells in Cancer
water as opposed to Pisaster or Pycnopodia water. T.brunnea
exhibited a flight response in the starfish waters but not in Cancer
water. T.pulligo exhibited a flight response to Pycnopodia, but not to
Pisaster or Cancer. T.montereyi displayed a flight response in
Pisaster water but was more stationary in Pycnopodia and Cancer
waters.
In the lab, T.brunnea was most susceptible to predation by
Pycnopodia. T.pulligo and T.montereyi, however, secreted a
distasteful pedal mucus that significantly decreased successful
predation by Pycnopodia. T.brunnea did not have such a defensive
mechanism.
None of the Tegula species displayed an active escape response
to the presence of Cancer. T.brunnea, however, was consumed least
often by Cancer because it had the thickest shell of the Tegula
species. T.pulligo, with an intermediate shell thickness, was
consumed at the greatest rate. T.montereyi, the thinnest shelled
species, had a lower than expected consumption rate, possibly
because of structural characteristics of its shell other than thickness.
Tegula and Benthic Predators
In response to Pisaster predation, fewer T.montereyi were
consumed than either T.pulligo or T.brunnea. These differences were
not significant and were not pursued further.
INTRODUCTION
Predation in natural habitats plays an important role in
structuring marine communities. Predation can determine the
abundance, variability, and distribution of species as well as provide
prey with strong selective pressures for the evolution of defensive
mechanisms that reduce predator-induced mortality. Prosobranch
gastropods have been particularly well-studied in this regard (Geller,
1982; Harrold, 1982; Schmitt, 1982; Shivji et al., 1983; Watanabe.
1984). These mechanisms can be classified as either avoidance
responses or general defense mechanisms.
Avoidance responses serve to limit encounters with predators.
These include camouflage coloration, lengthy withdrawal into shell,
or increased locomotion or climbing upon olfactory stimulation by
waterborne chemicals (Burke, 1964; Schmitt, 1981; Geller, 1982;
Palmer et al., 1982). The role of general defense mechanisms is to
reduce the probability of death once contact with a predator is made.
Common examples are morphologies that increase the prey's
handling time or chemicals to confuse the predator or render the
prey unpalatable (Barns, 1972; Herrlinger, 1983; Watanabe, 1983;
Palmer, 1985; Legault and Himmelman, 1993;). The intensity of
these responses has been shown to increase as the risk of predation
2
Tegula and Benthic Predators
increases (Legault and Himmelman, 1993). This paper explores the
variety of defensive adaptations of three species of subtidal Tegula
to three common benthic predators.
Three species of Tegula live on and around the kelp forests off
the central Californian coast. All are similar in size, diet, and external
shell morphology, but differ in abundance, distribution, and shell
strength (Abbott and Haderlie, 1980; Watanabe, 1983; Watanabe,
1984). T.brunnea, the most abundant snail, resides in low intertidal
and subtidal waters (0-6m), and has the thickest shell. T.montereyi,
rarest of the three species, inhabits off-shore kelp beds (7-12m) with
a majority of adults living on the lower half of kelp plants.
T.montereyi has the thinnest shell of the three species. T.pulligo has
a density close to that of T.brunnea, and is found in off-shore kelp
beds with T.montereyi. The shell thickness of T.pulligo is between
that of T.brunnea and T.montereyi.
Most known Tegula predators are benthic, the principal ones
being Pisaster giganteus and Pycnopodia helianthoides (Watanabe,
1984). Cancer antennarius also feed on Tegula, but less frequently
than do the starfishes. Pisaster is found in low intertidal areas, but is
most common in subtidal zones (Feder, 1980). Many gastropod
species respond to Pisaster by increasing locomotion away from the
sea star and increasing climbing rates (Szal, 1970; Schmitt, 1981,
1982; Harrold, 1982; Watanabe, 1983). Pycnopodia is less abundant
than Pisaster and occurs in subtidal zones. Cancer has a density
between that of Pisaster and Pycnopodia, and is generally found in
the intertidal zone and subtidally near the bases of kelp (Garth and
Abbott, 1980). Crushing predators generally prey upon thinner
Tegula and Benthic Predators
shelled gastropods and are thought to influence shell evolution in
areas where predation is high (Vermeij, 1978, 1987; Geller, 1982;
Palmer, 1985).
With a variety of simple experiments, this study attempts to
characterize avoidance and escape behaviors of each of the three
Tegula species to Pisaster, Pycnopodia, and Cancer. Additionally,
simple preferences by the predators for a particular Tegula species
based on snail palatability or shell morphology (other than shell
thickness which is examined with other defensive adaptations) will
be explored.
MATERIALS AND METHODS
This study was conducted at the Hopkins Marine Station of
Stanford University in Pacific Grove, California. All experimental
organisms were collected by SCUBA divers from the kelp forest
adjacent to the station and stored in outdoor tanks supplied with
running sea water. Organisms were given at least 24 hours to
acclimate to the tanks before use. Pycnopodia were given an
additional 24 hours to allow for the release of stomach contents.
Behavioral observations were made in three fiberglass outdoor
tanks (90 x 90 x 60 cm) and in two glass indoor aquaria (45 x 25 x
30 cm) each supplied with running sea water. All experiments were
carried out using Tegula with a maximum basal diameter of 19 to 28
mm. Pisaster giganteus ranged in sized from 17.5 to 27.2 cm (from
Tegula and Benthic Predators
tips of opposite rays), Pycnopodia helianthoides from 21.2 to 44.5
cm, and Cancer antennarius from 15.2 to 15.9 cm (carapace width).
Responses to Predator Scented Water
To examine whether Tegula can detect and differentiate among
predator species by detecting waterborne olfactory cues, snails were
observed in a 350 ml glass dish containing 175 ml of sea water from
various sources. Control sea water was obtained from the running
sea water system, and predator water was taken from tanks which
had held several individual predators for at least 72 hours. A total
of 10 snails of each species were observed in the 4 water types:
control, Pisaster, Cancer, and Pycnopodia water.
To begin, a single snail that had been gently handled until the
operculum fully closed was placed operculum side down in the
center of the dish. Only snails closing the operculum in less than 10
seconds were used in the experiment. These snails were then
observed for 10 minutes, noting the times when the epipodial
tentacles first appeared and when the snail had fully emerged and
attached its foot to the glass. Attachment was confirmed by
observing snails from below. The time between the appearance of
the epipodial tentacles and the sticking of the foot to the dish will be
referred to as the "shell emergence time." The location of each snail
was recorded after 10 minutes as being above the water line, at the
water line, or on the bottom of the dish. The shell emergence times
were analyzed by analysis of variance (ANOVA). The location of the
Tegula and Benthic Predators
snails after 10 minutes in different water types were analyzed by
Chi-square test.
Predation Rates
To test whether predation rates are different between the 3
Tegula species, snails were fed to predators in the outdoor tanks.
The consumption rates of snails fed to Pisaster and Pycnopodia were
calculated by counting, removing, and replacing empty shells daily.
Snails above the water line were knocked back into the tank.
Consumption rate for snails fed to Cancer was calculated by counting
the live snails remaining in the tank. These were then returned with
additional snails to keep the total number of each Tegula species
constant. Table I contains the specific numbers of organisms used in
each trial. The number of snails of each species eaten per individual
predator per day were analyzed by analysis of variance (ANOVA).
Additional Pycnopodia Experiments
To differentiate between effects of predator preferences and
effectiveness of prey escape responses, anesthesia was used to
eliminate escape responses. Two snails of each species were
submerged in isotonic MgCl2 solution for 90 minutes. They were
then added to an outdoor tank containing a single Pycnopodia.
Empty shells were removed daily. Snails remained inactive for the
duration of the experiment which lasted for 2 days.
Tegula and Benthic Predators
Predation of Tegula by Pycnopodia based on each species
palatability was investigated by feeding Pycnopodia extracted snails
The shells of six Tegula, two of each species, were opened, and the
foot and head of the snails removed. All six snails were placed in an
indoor aquarium containing a single Pycnopodia and feeding
behavior was observed.
The preference of Pycnopodia for Tegula species based on shell
characteristics was investigated by extracting one Tegula of each
species. The soft parts of each snail were then inserted into a shell of
a different Tegula species. T.brunnea was inserted into a shell of
T.montereyi, T.montereyi inserted into a shell of T.pulligo, and
T.pulligo was inserted into a shell of T.brunnea. The snails were
inserted so that the operculum blocked the shell aperture leaving no
snail tissue exposed. The shells were then placed in an indoor
aquarium containing a single Pycnopodia, and feeding behavior was
observed.
Finally, experiments were conducted to determine whether T.
montereyi and T. pulligo secrete a pedal mucus that is distasteful to
Pycnopodia. T.montereyi was held against the tube feet of
Pycnopodia for approximately 2 minutes, and then extracted from its
shell. The T.montereyi was then added together with an extracted
T.brunnea and T.pulligo, neither of which had been stimulated by a
predator, to an indoor aquarium holding a different Pycnopodia than
was used to stimulate the snail. Feeding behavior was observed.
This study was repeated, but with the stimulation of a T.pulligo
instead of a T.montereyi.
Tegula and Benthic Predators
Secretion of pedal mucus by live snails was tested by holding a
T.pulligo against the tube feet of Pycnopodia for approximately 2
minutes. The foot of the stimulated snail was then rubbed over the
shell and foot of a T.brunnea. This T.brunnea was added along with
an untreated T.brunnea to an indoor tank containing a single
Pycnopodia. Feeding behavior was only recorded if Pycnopodia
actively investigated the snails within two minutes of their deposit
into the tank and if at least 1 snail was consumed. Otherwise, the
trial was discarded to avoid artifacts resulting from loss or dilution of
the applied coating of mucus or from snail rejection due to a
nonforaging Pycnopodia. Three successful trials were carried out
with stimulation of T.pulligo, and 4 with T.montereyi. In 1 trial
involving T.montereyi, a third T.brunnea was treated with the mucus
from an unstimulated T.montereyi and added to the tank. Control
trials were conducted by feeding Pycnopodia 2 untreated T.brunnea.
Additional Cancer Experiments
To investigate movement as a possible escape response, 15
snails of each species were added to an outdoor tank containing 1
week-old crab water. After 100 minutes, the snails' location on the
sides or bottom of the tank was recorded. This test was repeated
once.
The response of Cancer to anesthetized snails was also
examined. One test included 3 crabs and 15 snails per species over 1
day. This test was repeated using only 2 crabs. A third trial
involved 5 snails per species and 1 crab.
Tegula and Benthic Predators
Taste preferences of Cancer were studied by feeding two
extracted snails of each species to a single crab in the indoor
aquarium. This test was repeated in the outdoor tank.
Finally, general observations of Cancer feeding on live snails
were made in the indoor tanks using one crab and 5 snails of each
species. Approximately 90 percent of the tank was covered in brown
butcher paper to limit visual distractions, and most observations
were made after dark using minimal lighting. Observations focused
on species selection, time held for each snail, and the condition of the
snail after release by the crab.
RESULTS
Responses to Predator Scented Water
Exposing Tegula to water with various predator scents elicits
specific avoidance responses from all 3 Tegula species. For both
T.brunnea and T.pulligo, the shell emergence times were significantly
greater in Cancer water compared to the control water and both
starfish species. Shell emergence times in starfish water were
shorter than in the control water, but these differences were not
significant for either snail species (Figs. 1-2; Table II). T.brunnea
and T.pulligo appear to detect Cancer water but not Pisaster or
Pycnopodia.
T. montereyi shell emergence time in control water was
significantly longer than that for either T.brunnea or T.pulligo
Tegula and Benthic Predators
(Pc.002), resulting in no significant difference between the
emergence times in the predator waters compared to the control
water for T.montereyi. However, shell emergence times in Cancer
water were still significantly longer than in either sea star water (Fig.
3; Table II)
Another measurement of avoidance response is characterized
by the snails’ movement in each of the water types. A significantly
greater number of both T.brunnea and T.pulligo climbed the side of
the glass dish in Pycnopodia water compared to the control water
(Figs. 4-5). A significantly greater number of T.brunnea also climbed
in Pisaster water compared to the control. T.pulligo did not show this
trend. Finally, neither T.brunnea or T.pulligo exhibited a significant
climbing difference in Cancer water compared to the control water
(Figs. 4-5).
Significantly more T.montereyi climbed in response to Pisaster
water compared to the control water. The differences between
Pycnopodia water and the control, and Cancer water and the control,
however, were not significant (Fig. 6).
In summary, T.brunnea has a longer shell emergence time in
Cancer water compared to the control, but the movement patterns
are not different. Emergence times were not affected in Pisaster and
Pycnopodia water, but increased climbing in these waters was
observed. T.pulligo is identical to T.brunnea, except that movement
was affected by Pycnopodia and not by Pisaster. T.montereyi's
response is less clear than the other Tegula species due in part to the
longer shell emergence time in the control water. No differences
between the control and predator waters were observed although
10
Tegula and Benthic Predators
there were differences between the Cancer and starfish waters.
Movement patterns were only affected by Pisaster.
Unbiased between-species comparisons of movement patterns
among the 3 Tegula species are not possible since the time before the
opening of the operculum was significantly longer for T.montereyi
than for either T.brunnea or T.pulligo (Appendix A & B). This left
T.montereyi less time than the other 2 species had to migrate to its
final preferred location before the end of the 10-minute experiment.
Pycnopodia Experiments
Of the 35 snails consumed by Pycnopodia during both
consumption trials, all but 2 were T.brunnea. Two T.pulligo and no
T.montereyi were consumed (Figure 7). Since snails above the water
line were knocked back into the tank, all species were assumed to be
equally available to the predators.
Investigating whether taste preference caused T.brunnea to be
consumed at the highest rate, snails of each species were extracted
from their shells and fed to Pycnopodia. In both trials, all snails,
regardless of species, were consumed within 5 minutes, suggesting
that Tegula palatability does not cause Pycnopodia to distinguish and
select between species.
The effect of shell type on consumption by Pycnopodia was
examined by extracting snails and inserting them into shells of
different Tegula species. Again, all snails were consumed, regardless
of species. This indicates that Pycnopodia do not distinguish among
snail species based solely on shell characteristics.
Tegula and Benthic Predators
Turning to the role of Tegula escape responses in surviving
Pycnopodia predation, snails were anesthetized and fed to the star.
Within 2 days, all snails were consumed in apparently random order
indicating the presence of escape behaviors in live T.montereyi and
T.pulligo.
The possibility of a mucus secretion by T.montereyi and
T.pulligo to deter predation was examined by extracting snails that
had been exposed to Pycnopodia tube feet and feeding the snails to
Pycnopodia. In both trials involving stimulated T.montereyi and
T.pulligo, all snails were eaten regardless of species, suggesting that a
mucus coating is not effective with dead snails.
Finally, pedal mucus secretion was studied by exposing
T.montereyi or T.pulligo to Pycnopodia and rubbing their mucus film
over the foot and shell of a T.brunnea. Of the 3 T.pulligo experiments
where Pycnopodia responded in less than 2 minutes, 2 trials resulted
in Pycnopodia consuming the untreated T.brunnea while actively
avoiding the one treated with mucus from T.pulligo. Both T.brunnea
were consumed in the third trial. Of the 3 T.montereyi experiments
where Pycnopodia responded in less than 2 minutes, 2 trials resulted
in Pycnopodia consuming the untreated T.brunnea and rejecting the
one treated with mucus from stimulated T.montereyi. The second of
these 2 trials included the T.brunnea treated with mucus from the
unstimulated T.montereyi, and it too was eaten. Both T.brunnea
were consumed in the third trial. In 4 control trials using 2
untreated T.brunnea, both snails were consumed by Pycnopodia.
Tegula and Benthic Predators
Cancer Experiments
The consumption data shows that Cancer ate T.pulligo
significantly more often than T.brunnea. T.montereyi was eaten
more frequently than T.brunnea, but these differences were not
statistically significant (Fig. 8; Table III). In the presence of MgClz,
all snails regardless of species were eaten at a significantly higher
rate. The rank order of the individual species, however, did not
change (Fig. 8; Table III). This indicates that behavioral responses
by Tegula species reduce predation by crabs, but that the
effectiveness is similar for all 3 species
Site selection by snails as a possible escape response was
investigated by recording the location of Tegula in the tank
containing Cancer water. The average of both 100-minute trials
reveals that the number of snails on the bottom and walls of the tank
is similar among the 3 Tegula species (Fig. 9). More snails were
found on the walls, away from where the crabs would be, than were
located on the bottom of the tank.
The selection of certain Tegula species based on Cancer
preference was studied by feeding extracted snails to the crabs.
In
both trials, all 6 snails, 2 of each species, were eaten within 10
minutes in no order. Cancer apparently do not select between
species based on snail palatability
To investigate further how Cancer selects its prey, feeding
behavior was observed and analyzed. Of the number of snails of
each species picked up by Cancer, the crabs attempted to consume
(either brought snail to mouth or tried to crack shell with chelipeds)
13
Tegula and Benthic Predators
a similar percentage from each species (Table IV). This shows a lack
of species selection by Cancer. Of the snails that Cancer tried to
consume, a greater percentage of T.pulligo and T.montereyi were
subsequently eaten than T.brunnea (Table IV). These data suggest
that Cancer consume the species with the thinnest and most easily
broken shells, those being T.pulligo and T.montereyi.
Pisaster Experiments
The data from the Pisaster eating trials reveal insignificant
differences between the consumption rates of the different Tegula
species (Figure 10; Table V). The low number of trials makes it
difficult to resolve differences in consumption rates.
DISCUSSION
Responses to Predator Scented Water
The detection of waterborne chemicals by the three Tegula
species varies between species. T.brunnea was able to detect all
three predators based on shell emergence times or movement
patterns. T..pulligo can detect Cancer and Pycnopodia, but not
Pisaster. T.montereyi, in contrast, appears to detect only Pisaster,
and not Cancer and Pycnopodia. Finally, all three Tegula species
seem to distinguish between Cancer and the starfish, but not
between the individual sea stars.
14
Tegula and Benthic Predators
That all three Tegula species take a significantly longer time to
emerge from their shells in Cancer water as opposed to Pisaster or
Pycnopodia water suggests that lengthy withdrawal into the shell is a
defensive behavior to Cancer. Lack of movement and exposure
might increase the chances of the shell appearing empty and being
bypassed by a foraging crab. This is supported by Vermeij (1987)
who reports that withdrawal into the shell helps snails avoid
detection by enemies and thwarts those attacking by way of the
aperture because soft parts cannot be easily reached. Additional
research into this behavior would be of value.
The number of each species of snails on the sides of the dish
does not increase in Cancer water compared to the control water.
This lack of active climbing supports the finding that gastropods are
unable to successfully flee from fast moving predators such as
Cancer, and therefore do not develop flight behaviors from them
(Schmitt, 1981).
The avoidance behaviors of individual Tegula species to
Pisaster and Pycnopodia water vary more than they did in Cancer
water. T.brunnea employs a flight response to Pisaster and
Pycnopodia as indicated by the increased climbing in these waters.
However, its high consumption rate by Pycnopodia in the laboratory
suggests this is not an especially effective response. T.pulligo
exhibits a flight response in Pycnopodia water, but not in Pisaster
water. With the exception of the lack of climbing by T.pulligo in
Pisaster water, these flight behaviors were expected because of the
slower movement speeds of the starfish. In the field, climbing gives
the snails a chance to gain safe refuge in kelp plants from slower
Tegula and Benthic Predators
moving predators (Watanabe, 1984). This then puts the snail in a
position where dropping off the substratum would give it a chance to
fall out of the reach of nearby predators (Watanabe, 1983). The lack
of active climbing by T.pulligo in response to Pisaster water cannot
be explained and further research would be of interest.
T.montereyi uses two different avoidance responses to Pisaster
and Pycnopodia water. Similar findings were reported by Herrlinger
(1983) and Watanabe (1983). In Pisaster water, significantly more
snails were found on the sides of the dish as compared to the control
water. In Pycnopodia water, however, T.montereyi did not show
differences in movement compared to the control water. This lack of
detection does not seem critical for survival since T.montereyi can
escape predation with a mucus secretion upon contact by
Pycnopodia, as will be discussed later.
Pycnopodia Experiments
T.pulligo and T.montereyi exhibited nearly flawless escape
responses to Pycnopodia predation in the laboratory. In contrast,
T.brunnea did not possess a defensive adaptation to survive
Pycnopodia. In the absence of escape behaviors, Pycnopodia did not
show a preference for one snail species over another. All dead snails,
regardless of species, were consumed. This indicates that the
different mortality rates between the Tegula species are indeed due
to the presence or absence of escape responses.
T.brunnea, whenever captured by a foraging sea star, was
consumed. The only exception was when its shell and foot was
16
Tegula and Benthic Predators
coated with mucus from a T.montereyi or T.pulligo that had been
stimulated by Pycnopodia. Stimulation was necessary for secretion
of the distasteful mucus as evidenced by the consumption of
T.brunnea coated with mucus from an unstimulated T.montereyi.
This supports the assertion that mucus secreted by T.montereyi and
T.pulligo in response to Pycnopodia is accountable for the snails
lower mortality rates (Watanabe, 1983; Herrlinger, 1983).
That T.montereyi survived Pycnopodia predation was not
surprising based on observations by Watanabe (1983). He reports
that T.montereyi allows its head and foot to contact the tube feet of
Pycnopodia when captured. This induces the starfish to reject the
snail as it did in my experiment. Herrlinger (1983) also observed
that Pycnopodia rejects T.montereyi when the snail is brought to the
mouth of Pycnopodia.
The use of distasteful mucus by T.pulligo to escape Pycnopodia,
however, has not been well documented. Herrlinger (1983) reported
that T.pulligo might secrete a distasteful mucus to lower consumption
rates by Pycnopodia. This behavior, though, was not investigated
further. In fact, previous field and laboratory observations of
interactions between T.pulligo and Pycnopodia indicate that T.pulligo
accounts for a major portion of Pycnopodia’s diet (Herrlinger, 1983:
Shivji et al., 1983; Watanabe, 1983). The different results of Shivji,
et al. (1983) can possibly be accounted for by the fact that their
observations took place off the coast of Vancouver where T.brunnea
is absent. Therefore, T.pulligo may have been the best prey species
available. The contradiction with Watanabe (1983) maybe a
consequence of maintaining constant abundances of each snail
17
Tegula and Benthic Predators
species in my laboratory experiments. In my tests, therefore,
Pycnopodia, preyed upon the least well defended species, T.brunnea,
and was not forced to attempt consumption of the other two species
as may have been the case in Watanabe’s (1983) experiments.
Unlike with the experiments by Shivji, et al. (1983) and
Watanabe (1983), the differences between my results and those of
Herrlinger (1983) cannot readily be accounted. Herrlinger (1983)
observed organisms in the same area from which my animals were
obtained. He found that Pycnopodia ate a much greater percentage
of T.pulligo than of either T.brunnea or T.montereyi, which were
hardly consumed at all. One explanation as to why more T.pulligo
are consumed in the field than T.brunnea is that T.pulligo are simply
more accessible to predation than are T.brunnea. T.pulligo survive in
subtidal kelp zones, but T.brunnea are mainly found in shallower
areas with a highly protective algal cover (Herrlinger, 1983;
Watanabe, 1984). This might make T.brunnea less accessible to
Pycnopodia forcing Pycnopodia to prey upon the more available
T.pulligo.
Cancer Experiments
T.brunnea had the most effective defense of the three Tegula
species against Cancer predation. In the absence of all active escape
responses, Cancer still consumed similar proportions of each Tegula
species. This indicates that the three snail species did not employ
active defensive behaviors that were different from one another.
Instead, a passive response, shell thickness, was effectively used by
18
Tegula and Benthic Predators
T.brunnea to lower mortality from predation. Although still
susceptible to Cancer predation, thicker shells are effective in
decreasing the potential food value of the snail by increasing its
handling time. Thick shells, however, are not desirable for all species
because they are expensive to make and may not be as functional
overall as some thinner shell types are (Vermeij, 1978, 1987; Palmer,
1985)
Focusing on the consumption of T.montereyi and T.pulligo, a
surprising finding was that more T.pulligo were consumed than
T.montereyi. T.montereyi have the thinnest shells and theoretically
should have been consumed at the highest rate. T.montereyi is not
distasteful to Cancer, since all extracted individuals were consumed.
One possible explanation for this discrepancy concerns shell
structure. Vermeij (1987) reports that crabs can be discouraged
from peeling a shell as the spirals get smaller and tighter together.
Furthermore, a deep umbilicus can lessen structural weaknesses of
shells. T.montereyi have the best defined umbilicals of the three
Tegula species which might account for its lower than expected
consumption rate. Additional research into this area would be of
value.
Pisaster Experiments
Pisaster consumed a higher number of T.brunnea and T.pulligo
than of T.montereyi over both feeding studies. No experiments were
conducted to identify possible defensive behaviors by T.montereyi
because the data were statistically insignificant. Previous studies,
19
Tegula and Benthic Predators
however, report that T.montereyi is indeed preyed upon less
frequently than are the other two species, probably because of its
ability to withdraw deeper into its shell (Vermeij, 1987; Watanabe
1983).
ACKNOWLEDGMENTS
I’d like to extend a special thanks to Jim Watanabe for his
direction, insight, and patience, and for setting aside his own
research to help me finish this project. My gratitude is also extended
to Joe Wible for aiding my research, and to all the Hopkins divers
who collected fresh organisms for me to manipulate and study.
Tegula and Benthic Predators
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Burke, W.R. 1964. Chemoreception by Tegula funebralis. Veliger
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Intertidal invertebrates of California. Stanford University Press,
Stanford, California, USA.
Geller, J.B. 1982. Chemically mediated response of a gastropod,
Tegula funebralis (A. Adams), to a predatory crab, Cancer
antennarius (Stimpson). Journal of Experimental Marine Biolog
and Ecology 65:19-28
Harrold, C. 1982. Escape responses and prey availability in a kelp
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Herrlinger, T.J. The diet and predator-prey relationships of the sea
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Legault, C., and J.H. Himmelman. 1993. Relation between escape
behavior of benthic marine invertebrates and the risk of predation.
Journal of Experimental Marine Biology and Ecology 170:55-74.
Tegula and Benthic Predators
Palmer, A.R. 1985. Adaptive value of shell variation in Thais
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1601
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936.
22
Tegula and Benthic Predators
Table I. Numbers of animals and length of trials for predation rate
experiments.
Predator
No. of
No. of
No. of
Trial
No. of
Species
Predators
Tbrunnea
T.montereyi
T.pulligo
No.
Pisaster
Pycnopodia
20
Cancer
snails were removed 2 days before end of trial to give Pycnopodia
stomach time to empty
Trial
Length
(days)
11
10
Tegula and Benthic Predators
Table II. Two-way ANOVA, showing the effect of snail species and predator
water type on length of time for snail to emerge from shell and grip
substratum.
ANALYSIS OF VARIANCE
Source
Sum-of-
Degrees of
Mean¬
F-Ratio
Probability
Freedom
Squares
Square
46.892
0.000
Snail
23.446
34.171
Species
Predator
67.645
22.548
32.862
0.000
13.465
0.005
Species X
2.244
3.271
Predator
ERROR
74.104
108
0.686
TUKEY POST HOC TEST
MATRIX OF PAIRWISE MEAN DIFFERENCES (Probabilities in Parentheses)
Tegula
Cancer
Pisaster
Pycnopodia
brunnea
Pisaster
-2.386 (.000
-1.654 (001)
0.733 (707
Pycnopodia
-1.311 (.028)
0343 (999)
Control
1.075 (155
Tegula
Cancer
Pisaster
Pycnopodia
montereyi
-1.542 (004)
Pisaster
-1.383 (015)
0.159 (1.000
Pycnopodia
0.746 (684)
Control
0.637 (855)
0.797 (588)
Tegula
Cancer
Pisaster
Pycnopodia
pulligo
-1.880 (.000
Pisaster
-1.821 (.000
0.059 (1.000
Pycnopodia
2.579 (.000)
0.758 (662)
0.699 (765)
Control
24
Tegula and Benthic Predators
Table III. Two-way ANÖVA, showing the effect of snail species and MgClz on
Tegula consumption rate by Cancer.
ANALYSIS OF VARIANCE
Source
Sum-of-
Degrees of
F-Ratio
Probability
Mean¬
Squares
Freedom
Square
Snail
7.142
10.664
5.332
0.014
Species
6.400
6.400
8.573
0.017
Mgcl
Species X
0.339
0.253
0.506
0.721
MgCl2
6.719
ERROR
0.747

TUKEY POST HOCTEST
MATRIX OF PAIRWISE MEAN DIFFERENCES (Probabilities in Parentheses)
Cancer
T.brunnea
T.montereyi
antennarius
0.764 (396
T.montereyi
2.083 (012
1.319 (097
Tpullige
—
Tegula and Benthic Predators
Table IV. Observed selection and consumption of Tegula by Cancer.
Snails Eaten
Snail Species
Consumption Attempts
Snails Captured
Consumption Attempts
67%
T.brunnea
60%
T.montereyi
22%
T.pullige
67%
25%
Tegula and Benthic Predators
Table V. One-way ANÖVA, showing effect of snail species on consumption
by Pisaster.
ANALYSIS OF VARIANCE
Sum-of-
Source
Degrees of
Mean¬
Probability
F-Ratio
Freedom
Square
Squares
3.108
0.186
Snail
0.073
0.036
Species
ERROR
0.035
0.012
TUKEY POST HOCTEST
MATRIX OF PAIRWISE MEAN DIFFERENCES (Probabilities in Parentheses)
Pisaster
T.brunnea
T.montereyi
giganteus
-0.254 (192)
T.montereyi
0.206 (281)
0.047 (903
T.pulligo
—
Tegula and Benthic Predators
Figure Legends:
Figure 1. T.brunnea: Average time from opening of operculum to
sticking of foot in different water types.
Figure 2. T.pulligo: Average time from opening of operculum to
sticking of foot in different water types.
Figure 3. T.montereyi: Average time from opening of operculum to
sticking of foot in different water types.
Figure 4. Distribution of T.brunnea after 10 minutes in different
water types.
Figure 5. Distribution of T.pulligo after 10 minutes in different
water types.
Figure 6. Distribution of T.montereyi after 10 minutes in different
water types.
Figure 7. Average number of each snail species eaten per day per
Pycnopodia.
Figure 8. Average number of each snail species eaten per day per
Cancer.
Figure 9. Average distribution of snails in Cancer water after 100
minutes.
Figure 10. Average number of each snail species eaten per day per
Pisaster.
300
200
100 :
0

Water Types
Tegula and Benthic Predators
Control Water
Pisaster Water
Cancer Water
□ Pycnopodia Water
Figure 1.
300 7
200
100 -
0 +



Water Types
Tegula and Benthic Predators
Control Water
Pisaster Water
□ Cancer Water
□ Pycnopodia Water
Figure 2.
Figure 3.
400
300 -
200 -
100 -
Tegula and Benthic Predators
Control Water
Pisaster Water
□ Cancer Water
□ Pycnopodia Water
Water Types
Tegula and Benthic Predators
Figure 4.
12 7
Bottom
At Water Line
□ Above Water Line
A
Pycnopodia
Control
Pisaster
Cancer
Water Type
Chi-Square Values (Probabilities in Parentheses)
Control vs. Pisaster
6.667 (0.010)
Control vs. Cancer
0.000 (1.000)
Control vs. Pycnopodia
6.667 (0.010)
32
Tegula and Benthic Predators
Figure 5.
87
Bottom
At Water Line
Above Water Line




Pisaster
Pycnopodia
Contro
Cancer
Water
Type
Chi-Square Values (Probabilities in Parentheses)
Control vs. Pisaster
2.095 (0.351)
Control vs. Cancer
1.818 (0.403)
Control vs. Pycnopodia
6.921 (0..031)
33
Tegula and Benthic Predators
Figure 6.
10
Bottom
AtWater Line
□ Above Water Line


L
oA
Contro
Pisaster
Cancer
Pycnopodia
Water Type
Chi-Square Values (Probabilities in Parentheses)
Control vs. Pisaster
7.200 (0.027)
5.067 (0.079)
Control vs. Cancer
Control vs. Pycnopodia
1.067 (0.587)
34
Figure 7.
2.0-
50
5210
O.O-

Trial1
Tegula and Benthic Predators
Tbrunnea
T.montereyi
E T.pulligo
Average

Trial 2
Totals
Figure 8.
4.0
Tegula and Benthic Predators
Tbrunnea
T.montereyi
E T.pulligo
0.0
Average of Trials with
Normal Snails
Average of Trials with
Anesthetized Snails
Totals
36
Figure 9.
10.0-
8.0-
6.0
4.0
0.0-
Bottom
nea
ereyi
Location
Tegula and Benthic Predators
Figure 10.
0.6
0.5
0.4:
O.3
52
0.2
0.1
0.0-
2
Trail1
Tegula and Benthic Predators
T.brunnea
T.montereyi
E T.pulligo
Trial.
Totals
Tegula and Benthic Predators
Appendix A.
Average Time for the Operculum of Each
Snail Species to Open in the Different
Water Types
150 +
T.brunnea
T.montereyi
E T.pullige
Z



Pisaster
Control
Cancer
Pycnopodia
Water Type
39
Tegula and Benthic Predators
Appendix B. Two-way ANOVA, showing the effect of snail species and
predator water type on length of time for Tegula
epipodial tentacles to appear.
ANALYSIS OF VARIANCE
Sum-of-
Source
Degrees of
Mean¬
F-Ratio
Probability
Squares
Freedom
Square
111.595
Snail
55.797
77.690
0.000
Species
Predator
14.055
4.685
0.000
6.523
Species X
9.962
0.039
1.660
2.312
Predator
ERROR
77.565
108
0.718
TUKEY POST HOCTEST
MATRIX OF PAIRWISE MEAN DIFFERENCES (Probabilities in Parentheses)
Control
T.brunnea
T.montereyi
water
T.montereyi
1.700 (0.001)
-1.117(0.139)
2.817 (0.000)
T.pulligo
Pisaster
T.brunnea
T.montereyi
water
T.montereyi
1.334 (0.030)
T.pulligo
0.745 (0.715)
-2.079 (0.000)
Cancer
T.montereyi
T.brunnea
water
1.168 (0.101
T.montereyi
0.588 (0.923)
-1.755 (0.001)
T.pulligo
Pycnopodia
T.brunnea
T.montereyi
water
2.665 (0.000)
T.montereyi
2.403 (0.000)
0.263 (1.000
T.pulligo
40
Tegula and Benthic Predators
Appendix C. Consumption data of trials with Pycnopodia
helianthoides.
Trial
NUMBER CONSUMED
Trial 2
Trial 1
Length
T.brunnea
T.montereyi
T.pulligo
T.brunnea
T.montereyi
T.pulligo
(days)
10
13
20
Total
Tegula and Benthic Predators
Appendix D. Consumption data of trials with Cancer antennarius.
Active Snails
NUMBER CONSUMED
Trial
Trial 2
Length
Trial 1
T.pulligo
T.brunnea
T.montereyi
T.pulligo
T.brunnea
T.montereyi
(days)
16
Total
33
2
Anesthetized Snails

Trial
NUMBER CONSUMED
Length
Trial 1
Trial 2
T.montereyi
Tbrunnea
T.montereyi
T.pulligo
T.brunnea
T.pulligo
(days)
10
Total
Anesthetized Snails
Trial
NUMBER CONSUMED
Trial 3
Length
T.brunnea
T.montereyi
T.pulligo
(days)
Total
Tegula and Benthic Predators
Appendix E. Consumption data of trials with Pisaster giganteus.
NUMBER CONSUMED
Trial
Trial 1
Trial 2
Length
T.montereyi
T.brunnea
T.montereyi
T.brunnea
T.pulligo
T.pulligo
(days)
10
11
Total
13
18
12