Download Prey species use a variety of mechanisms to escape from their

J. Exp. Mar. Biol. Ecol., 1983, Vol. 71, pp. 257-270
257
Elsevier
ANTI-PREDATOR
CONTRASTING
DEFENSES OF THREE KELP FOREST GASTROPODS:
ADAPTATIONS
OF CLOSELY-RELATElD
PREY SPECIES
JAMES M. WATANABE’
Department of Zoology, University of California, Berkeley, CA 94720. U.S.A.
Abstract: The defensive adaptations of three species of Tegula that inhabit kelp forests along the central
California coast were investigated. Their principal predators are the starfishes P&aster giganteus (Stimpson)
and Pyc~opodia heia~tho~de~(Brandt). Tegtda brwmea (Philippi) relies on avoidance and flight to escape from
both species of starfish. Te~~apul~igo (Gmelin) flees from contact with Pisaster, but not Pycnopodia. When
attacked by the latter species, Tegula pulligo clamps its shell down against the substratum. T. montereyi
(Kiener) possesses the most effective defenses of the three turban snail species. It flees from P&aster. When
captured, it withdraws quickly and deeply into its shell, which is larger (relative to body dry weight) than
those of the other two species. This withdrawal caused Tegula montereyi to be rejected by Pisaster more often
than the other two species, possibly through erroneous decisions by the starfish that the shell was empty.
Teguta montereyi does not withdraw into its shell when captured by Pycnopodia; observations indicate that
Tegula montereyi may be distasteful to Pycnopodia. Despite the close taxonomic relationship of the three
Tegzda species and their similar ecological requirements, defensive responses to their principal predators
differ. In addition, two of the three species appear to distinguish between the two starfish species and
respond in a different manner to each.
INTRODUCTION
Prey species use a variety of mechanisms to escape from their predators, Defenses
include avoidance and flight (e.g. Bullock, 1953; Feder, 1963; Phillips, 1975; Schmitt,
19811, mo~holo~c~
sp~i~zations
(Vermeij, 1978; Moitoza & Phillips, 1979),
noxious secretions (Thompson, 1969; Nance & Br~thw~te, 1979), homing to a semipermanent shelter site (Car&y & Levings, 1983), camouflage (Bloom, 1975; Vance,
1978; Fishlyn & Phillips, 1980) and aggressive counterattacks (Pratt, 1974; Harrold,
1982). One approach to understanding this diversity of defensive mechanisms is to
examine the defenses of closely related, sympatric prey species that are consumed by
the same predators (Sch~tt, 1981). The present paper describes contrasting defenses
of three congeneric species of kelp forest gastropods against two of their principal
predators.
Three species belonging to the genus Tegulu occur along the coast of central
California, U.S.A. Commonly known as turban snails, the three species are similar in
size, external shell mo~holo~, and diet. However, they differ in bath~e~c
distribu-
’ Present address: Hopkins Marine Station, Stanford University, Pacific Grove, CA 93950, U.S.A
0022-0981/83/%O3.00 0 1983 Elsevier Science Publishers B.V.
258
JAMES M. WATANABE
tion and abundance (Riedman et al., 1981; Watanabe, 1982): T. brunnea (Philippi) is
abundant and occurs in low intertidal and shallow subtidal zones (O-6 m). T. p&go
(Gmelin) is roughly equal in overall density to T. b~n~u~ but occurs pr~ominantly in
deeper water (7-12 m). The third species, T. montereyi (Kiener), is relatively rare and
has a bathymetric distribution similar to that of T. p&go. Benthic predation restricts
T. brunnea to shallower depths and affects habitat use of the other two species
(Watanabe, in press).
The principal benthic predators of Z’egufu in central California are the starfishes
Pisustergigunteus (Stimpson) and Pycnopodiu heziunt~ojdes(Brandt). Gastropods occur
frequently in the diets of both species in central California (Harrold, 198 1; T. Herrlinger,
pers. comm.). Pisuster generally feeds by everting its cardiac stomach against its prey.
Snails the size of adult Tepla (20-25 mm) can only be digested one at a time, although
multiple prey can be captured and held. ~ycno~od~uingests its prey and is thus able to
digest multiple prey s~ult~eously.
Hunt (1977) observed a single Pycno~odia attack
and consume 11 Tegula in a 35min period.
This paper shows that despite the close relationship of the three Teguiu species and
the similarity of their two major predators, the effectiveness of their anti-predator
adaptations differ markedly, The most well-defended species T. montereyi, employs very
different defenses against each starfish, requiring that it be able to identify the attacking
species accurately and quickly and make the appropriate response.
MATERIALS
AND METHODS
The research was conducted at the Hopkins Marine Station of Stanford University,
Pacific Grove, California, U.S.A. (36”36’N: 121”54’W). Experimental animals were
collected from the kelp forest adjacent to the Station. All laboratory experiments were
conducted in large outdoor tanks supplied with running sea water.
Behavioral responses of snails to contact with the two predator species were made
in the laboratory and the field. Laboratory observations were made in glass-walled
aquaria containing one predator and several individual snails, Encounters were
observed without disturbing the animals. In the field, a starfish was brought close to
a previously undisturbed snail so that only the tube feet touched the snail’s foot,
epipodial tentacles, or cephalic tentacles. Responses to initial and repeated contacts
were noted. No attempt was made to quantify long-dist~ce responses of snails to
starfish during this study.
RELATIVE
SUSCEPTIBILITY
The relative susceptibilities of the three Tegzdu species to capture by each of the
starfishes were dete~ned
in the laboratory. Fifteen indi~du~s of each snail species
were placed with either four Pisuster or two Pycnopodia in a large tank (90 x 90 x 60 cm)
for 5 days. Three replicate experiments were carried out for each starfish species using
GASTROPOD
ANTI-PREDATOR
DEFENSES
259
freshly collected snails and starfish each time. Individual snails ranged from 16.1 to
25.5 mm (maximum basal diameter). Pisuster ranged in size from 14 to 18 cm (inter-ray
to opposite ray tip) and ~yc~~~~~~ from 30 to 40 cm (diameter).
The tanks were examined several times per day. Empty shells released by starfish
were removed from each tank and measured. Consumed snails were not replaced.
Because Pycnopodia ingests its prey, starfish of this species were kept in a tank without
prey for 1 to 2 days before and after the ex~rjments. This protocol ensured that their
guts were empty at the beginning of each experiment and that ail individual prey
consumed during the experiments were counted.
DIGESTION
TIMES
Digestion times of the different Teguiu species were determined only for Pimster
giganteus. Starfish and snails were collected from the field immediately before each
experiment. Snails were fed to starfish by holding them in front of a ray tip until the
starfish had firmly grasped the shell with its tube feet. Digestion time was measured as
the time from initiation of feeding (i.e. when the starfish had brought the snail to its
mouth with the shell’s aperture against its mouth) until release of the empty shell.
Not ail starfish fed in the laboratory. Because tank space was limited, starfish that
fed consistently were sometimes used more than once. However, starfish that were used
more than once were fed different species of snails each time.
Starfish were fed snails that were either anesthetized in MgCl, or not. Fifteen
unanesthetized and seven anesthetized individuals of each species were fed to Pisuster
(N = 5 anesthetized snails for Tegulapulligo). Differences in digestion times between the
two conditions indicated whether a snail’s ability to withdraw into its shell is any
deterrent to predation by starfish. Adult snails ranging from 19.5 to 23.0 mm were used
in these experiments. The presence of MgCl, did not appear to inhibit feeding by the
starfish.
SHELL CHARACTERISTICS
The laboratory studies concentrated
on the susceptibilities of the snail species to
extracting predators (i.e. starfish). However, crushing predators, such as crabs and
demersal fishes, also consume Tegula (Hunt, 1977). I investigated the relationships
between shell weight, shell volume and soft part dry weight of the three Tegulu species
to determine if their potential susceptibi~ties to crushing predators differ.
Fifty-two individuals of each species were collected in July 1982. Basal diameter and
height of each shell were’measured to the nearest 0.1 mm. Each snail was then cracked
open and the soft parts and shell fragments air-dried to constant weight. Both portions
were weighed to the nearest mg. Snail sizes ranged from 8.6 to 25.0 mm for Tegda
bmnnea, from‘8.2 to 25.5 mm for T. montereyi%and from 6.5 to 25.5 mm for 7”.pulligo.
Shell volumes were estimated using the formula for a cone (xr2h)/3. Shells of the three
species are similar in shape so that no strong biases were likely to have been introduced
260
JAMES M. WATANABE
by estimating volume in this manner. In addition, snails with noticeably eroded shells
were not used in these analyses.
Linear regression equations of body dry weight vs. shell volume and shell volume vs.
shell weight were calculated for each species (Sokal & Rohlf, 1969).
RESULTS
RELATIVE SUSCEPTIBILITY
Pisaster consumed a significantly higher proportion of Tegulapufligo than either of the
other snail species (Table I). However, more than a third of the individuals of each
TABLE I
Percent mortality of Tegula in laboratory susceptibility experiments: 15 individuals of each snail species
placed with four Pisaster or two Pycnopodia for 5 days; n = 3 replicates for each starfish species; ranges of
percent mortality in parentheses.
Pisaster
giganteus
Pycnopodia
helianthoides
Tegula pulligo
88.9%
(73-100)
50.9%
(33-69)
Tegula brunnea
65.3 y0
(60-69)
70.6%
(67-78)
Teguia montereyi
54.3 %
(43-60)
(O-7)
Student-Newman-Keuls”
test
Pisaster:
Pycnopodia:
2.2%
Tp
Tb
Tb
Tp
Tm
Tm
a ANOVA of percent mortality for each starfish species conducted on arcsin-transformed data. Mortalities
of snail species that are underlined are not significantly different (P > 0.05, Student-Newman-Keuls
test).
species were consumed during each 5-day experiment, indicating that Pisaster readily
eats all three species.
Pycnopodia attacked and consumed substantial numbers of Tegula brunnea and
T. pulligo. However, only one individual T. montereyi was eaten by the six different
starfish during the three replicate experiments (Table I). Pycnopodia actively avoided
Tegula montereyi. Frequently Pycnopodia captured an individual Tegula montereyi,
brought the snail to its mouth and then dropped it. In most instances the starfish
continued to forage, captured a snail of a different species and immediately ingested it
(see below for further details).
BEHAVIORAL OBSERVATIONS
In the laboratory experiments, the three TeguZa species were not equally susceptible
to the two starfish. One factor that contributed to differences in mortality rates was
variation in escape responses of the snails.
GASTROPOD ANTI-PREDATOR
DEFENSES
261
Responses of Tegula brunnea
Tegula brunnea responded in a similar manner to contact with Pisaster and Pycnopodia
(Table II). When the epipodial tentacles or the side of the foot were touched by a
starfish’s tube feet, the snail turned away from the point of contact and moved off at
an increased speed. If contact was made head-on or on the cephalic tentacles, the snail
recoiled, lifted the anterior portion of the foot off the substratum, turned quickly away
from the point of contact (often > 90” to the previous direction of travel) and moved
quickly away. These behaviors (i.e. turning away and moving off at an increased speed)
will be referred to as the avoidance response and the flight response.
If contact with the starfish or its tube feet continued, snails often responded by
shell-twisting, a violent rotation of the visceral mass and shell from side to side. During
the early stages of an attack, shell-twisting sometimes broke the grip ofa-starfish’s tube
feet, allowing the snail to escape.
Snails attacked while crawling on vertical surfaces responded by moving upward
quickly. In laboratory aquaria, snails moved to the air-water interface and continued
to move laterally, sometimes with the shell partially out of the water. Snails unable to
escape in this manner often shell-twisted and dropped off the substratum simultaneously.
Dropping-off was usually a successful escape tactic unless the starfish had already
gripped the shell with many tube feet. If escape was unsuccessful, snails continued to
try to move away until the starfish pulled them off the substratum prior to initiation of
feeding. Snails withdrew quickly into their shells once contact with the substratum had
been broken.
Responses of Tegula pulligo
Tegula pulligo responded
to contact with Pisaster in a similar manner as Tegula
with this species, T. pulligo consistently avoided and fled
(Table II). Continued contact caused shell-tv,jsting and dropping-off (if the snail were
attacked while on a vertical surface). As with T. brunnea, attempts to escape continued
until the snail was removed from the substratum by the starfish. Once this occurred,
snails withdrew rapidly into their shells.
Contact with Pycnopodia did not consistently evoke avoidance and flight of Tegula
pulligo. On horizontal surfaces, snails often responded to contact with Pycnopodia by
withdrawing the head and clamping the shell against the substratum. Starfish sometimes
walked over clamped-down snails without attacking, but numerous Tegula pulligo that
clamped down were consumed during the laboratory experiments. From observations
through the walls of glass aquaria, clamped-down snails that were captured withdrew
quickly into their shells once they had been removed from the substratum. On vertical
surfaces, T. pulligo responded to contact with Pycnopodia by dropping-off. In contrast
to this species’ reactions to Pisaster, shell-twisting in response to contact with Pycnopodia
was rarely observed.
brunnea. Upon contact
Off
Drop-
Behavioral
Shell
twist
TABLE II
Avoid
++
++
++
++
++
++
<
Flight
of response
to Pisaster
intensity
Response
_
_
Clamp.
down
Tegula
brunnea
Tegula
pulligo
Tegula
montereyi
of Tegulu to Pisasfer and Pycnopodia: + + , response always observed;
_ , response not observed.
Increasing
<
responses
+
+
Clamp
down
+ , response
f
+
f
f
++
++
intensity
Flight
Increasing
Avoid
>
*
k
+
Shell
twist
of response
l
f , response
to Pycnopodia
observed;
Response
frequently
relatively
+
+
+
Off
Drop-
rare;
K
5
2
S
GASTROPOD
ANTI-PREDATOR
263
DEFENSES
Responses of Tegula montereyi
Tegula montereyi responded to contact with Pisaster by avoiding, tleeing, and some-
times shell-twisting. On vertical surfaces, snails moved upward quickly and dropped-off
if contact with tube feet continued (Table 11). Once a snail was captured by Pisaster,
it withdrew quickly into its shell.
Initial responses to attacks from Pycnopodia were similar to those of Tegura pulligo:
snails crawling on vertical surfaces avoided the predator and dropped-off, snails on
horizontal surfaces sometimes fled but more often clamped-down. If captured by
Pycnopodia and removed from the substratum, snails pulled slowly into their shells.
However, unlike the other Tegufa species, snails often reemerged before being ingested
by the starfish, exposing the foot and head to the starfish’s tube feet and oral area. At
this point, Pycnopodia usually rejected the snail and released it from its tube feet. The
re-emergence of the snail was not accompanied by violent twisting or aggressive biting
of the starfish; contact with the snail’s soft parts appeared to be the stimulus for
rejection. Once it had been rejected, the snail remained out of its shell and usually moved
slowly away from the starfish (see below for further discussion).
DIGESTION
TIME
The amount of time required by Pisaster to digest the different Tegula species ranged
from 10 to 19 h. There were no significant differences in mean digestion times of the
three species (unanesthetized snails; analysis of variance, P > 0.75) (Table III).
There were no significant differences in digestion times between anesthetized and
unanesthetized snails of the same species (Table III). Digestion of Tegufa by Pisaster
does not appear to be significantly slowed by closing the shell with the operculum.
Pkaster rejected Tegula montereyi more frequently than it did the other two species
during the digestion experiments (Table IV). This result was somewhat unexpected,
since Pisaster consumed substantial numbers of all three species in the susceptibility
TABLE I11
Digestion times of Tegu/a by Piraaer: mean time in hours from capture to release of empty shell; numbers
in parentheses are sample sizes followed by 95% confidence interval; digestion times of anesthetized and
unanesthetized conspecifics compared using f-tests; digestion times of the three snail species were not
significantly different from one another (unanesthetized snails, ANOVA, P > 0.75).
Unanesthetized
.-~~
MgCl,
-.-.
r-test
-P = 0.90
.-
Tegda brunnea
12.6
(14, 0.98)
12.5
(7, 2.16)
Tegda monrereyi
14.7
(4, 2.74)
13.7
(7, 2.35)
P = 0.50
Tegula pulligo
14.3
(II, 1.37)
12.4
(6, 1.37)
P = 0.15
.-
JAMES M. WATANABE
264
experiments (Table I). However, in 11 of 15 trials in which TeguZu montereyi was fed to
dropped the shell without consuming the snail.
Similar rejections occurred in only 4 of 15 trials with TeguZapu~i~goand in only 1 of
15 trials with T. brurmea (Table IV).
Pisaster, the starfish subsequently
TABLE
IV
Rejection of TeguIu by Pisaster: percent of snails captured in the laboratory, brought into feeding position
and subsequen~y dropped without being eaten; n = If unaues~etized snails of each species and seven
anesthetized snails (n = 6 for T. ~~~~jgu).
Tegula montereyi
Tegula p&go
Tegula brunnea
Unanesthetized
(%)
__.
73.3
26.7
6.7
MgC&
(%)
0.0
0.0
0.0
Individual T. montereyi withdrew rapidly into their shells when captured by Pisaster.
Starfish examined the shell aperture with the oral tube feet before attempting to feed
(i.e. everting the cardiac stomach). If the snail had pulled s~ciently far into its shell,
the starfish may have sensed erroneously that the shell was empty and rejected the snail.
The decision to reject the snail usually occurred within half an hour of capture. In two
cases, individual Tegula montereyi were held by Pisaster for 15 and 16 h without being
digested.
Rejected TeguZa mont~reyi were pulled extremely far into their shells. The operculum
was barely visible around the columella and the shell at first appeared to be empty.
Those snails that were held by starfish for less than half an hour emerged from their
shells within an hour of rejection and appeared to be unharmed. Both snails that were
held for more than 15 h were intact but appeared to be dead.
Pisaster never rejected snails that were anesthetized in MgCl, (Table IV), indicating
that rejection was probably caused by an active behavioral response rather than
unpalatability of the snail.
SHELL CHARACTERISTICS
The relationships between shell volume and shell weigbt and body dry weight and
shell volume differ among the three Tegda species. For both relationships, the slopes
of the regression lines for the three species are significantly different (Table V;
P < 0.001, F-test; Sokal & Rohlf, 1969). An analysis of covariance is therefore
inappropriate, but the following trends can be seen.
From the relationship between body dry weight and shell volume, Tegulu montereyi
tends to have a larger shell for a given body weight than the other two species (Table V).
The difference becomes more pronounced among larger snails. These findings corroborate the data on rejection of T. montereyi by Pisaster: Tegula montereyi has a larger
GASTROPOD
ANTI-PREDATOR
265
DEFENSES
shell, giving snails a larger volume into which they can withdraw. This in turn appears
to lead to more frequent rejection by PzLrusterthrough erroneous decisions that the shell
is empty. Shell volumes of the other species do not increase as rapidly with increasing
body weight, indicating that these species have relatively less shell volume into which
they can withdraw.
TABLE V
Regression equations for leg& shell characteristics: volume in mm3; weight in mg; n = 52 snails of each
species; 95% confidence interval in parentheses.
Shell volume (Y) vs. body dry wt (X)”
Tegula montereyi
f = 7.375X + 112.34
(0.330)
(80.36)
6.774X+
(0.337)
115.32
(74.98)
Tegula pulligo
f =
Tegula brunnea
f = 6.285X + 48.72
(0.301)
r2 = 0.98
12 = 0.97
r* = 0.97
(68.51)
Shell wt (Y) vs. shell volume (X)b
Tegula montereyi
90.26
(65.97)
r2 = 0.97
f = 0.819X + 51.74
r* = 0.95
f = 0.740X +
(0.035)
Tegula p~Il~g0
(0.052)
Tegda brunnea
f =
(82.84)
1.224X - 22.03
(0.47)
(68.63)
r2 = 0.98
a Slope for T. montereyi significantly greater than for the other two species.
b All slopes signific~tly different (P < 0.~1).
Among larger snails with the same shell volume, Tegula brunnea has the heaviest shell
of the three species and T. montereyi the lightest. Shell weight may not necessarily
reflect resistance to crushing predators (especially those that peel shells from the
aperture). However, these three species of Tegda do not possess thickened or toothed
shell apertures. Because shell thickness of the body whorl (in~lud~g the lip) is fairly
uniform for each species, shell weights are probably good estimates of relative resistance
to crushing and peeling predators. Qualitative estimates of shell strength (i.e. resistance
to cracking in a small vise) corroborate these findings: the shell of T. brunnea is the
hardest to crack, that of T. montereyi the easiest.
DISCUSSION
DEFENSES
OF TEGULA
Despite their close taxonomic relationship, the anti-predator tactics of the three
Tegdu species differ in the types of defenses employed and their effectiveness against
the two predator species. The defenses of T. brunnea and T.pulligo axe primarily
behavioral, while T. montereyi also employs morphological and possibly chemical
mechanisms.
266
JAMES M. WATANABE
Tegula brunnea
The responses of T. brunnea to Pisaster and Pycnopodiu are very similar. Studies of
the reaction of Tegulu brunneu to the intertidal starfish, Pisuster ochruceus (Brandt), have
described the same range of responses that I observed to subtidal predators (Bullock,
1953; Feder, 1963). Snails avoid, flee, shell-twist and drop-off in response to all three
starfish. Unlike the other two Tegufu that I studied, T. brunneu does not appear to
distinguish among the different predators. However, it can distinguish between predators and non-predators (Feder, 1963).
At the present time, starfish are the primary predators of turban snails in the
Monterey Bay area (see Watanabe, in press). However, prior to the re-expansion of sea
otter populations in central California, crushing predators (e.g. Cancer untennurius) were
more abundant and consumed turban snails (D.P. Abbott, pers. comm.). Teguh
brunneu may be the best defended of the three Tegulu against crushing predators,
although no data were gathered in the present study to address this possibility (see
Abbott & Haderlie, 1980).
Tegula pulligo
Tegulu pulligo was the most susceptible snail species to Pisuster in the laboratory
experiments, even though its defensive responses were similar to those of the other two
Tegulu. The bathymetric distribution of T. pulligo overlaps more with Pisuster than do
those of either Tegulu brunneu or T. montereyi (Watanabe, in press). Field experiments
have shown that T. pulligo spends more time on kelp plants (where starfish do not
forage) and very little time on the primary substratum (Watanabe, in press). Mortality
is reduced by (1) avoiding areas where encounters with predators are more likely, and
(2) active flight if such encounters occur. Such passive strategies (sensu Ansell, 1969)
have been documented for a number of other marine invertebrate species (e.g. Fawcett,
1979; Nelson & Vance, 1979; Garrity & Levings, 1981; Schmitt, 1982).
Why T. pulligo lacks a flight response to Pycnopodiu is not clear. A high proportion
of T. pufligo were eaten by Pycnopodiu in the susceptibility experiments, indicating that
the clamp-down response is not very effective (at least under artificial laboratory
conditions). In the laboratory, Pycnopodiu does not ignore clamped-down Teguh pufligo
as if its shell were chemically camouflaged, which has been inferred for the intertidal
limpet Notoucmeu pufeuceu (Fishlyn & Phillips, 1980). One factor could be the greater
speed of Pycnopodiu relative to Pisuster. I have often observed Tegulu outrunning
foraging Pisuster, but not the faster-moving Pycnopodiu. However, it seems that a flight
response that only rarely succeeds would have some selective advantage over no
response at all. Field studies, where predator and prey are not confined to an artificially
restricted space, are necessary to evaluate the true effectiveness of the clamp-down
response.
GASTROPOD
ANTI-PREDATOR
DEFENSES
267
Tegula montereyi
Teg& montereyi has the most effective defenses of the three Tegulu species against
both starfish species. T. montereyi flees when attacked by Prkaster and if captured, it
escapes through rapid and deep withdrawal into its larger shell. A similar morphological
defense of the intertidal turban snail, Tegula funebralis, against Pisaster ochruceus was
described by Markowitz (1980). Smaller snails can withdraw farther into their shells.
Intact individuals were rejected by starfish significantly more often than snails whose
shell lips had been filed back to the operculum.
The primary defense of Tegula montereyi against Pycnopodiu appears to be distastefulness, although further work is required to substantiate this possibility. When captured
by Pycnopodiu, Tegula montereyi allows the head and foot to contact the starfish’s tube
feet, which usually leads to rejection. Where distastefulness has been inferred as an
anti-predator defense in marine gastropods, defensive chemicals are often derived from
diets (e.g. Stallard & Faulkner, 1974; Ambroseet al., 1979). However, in the laboratory,
diets of the three Tegula appear to be very similar (Watanabe, 1982). If the apparent
distastefulness of T. montereyi is derived from its diet, it is not clear why the other two
species are not also distasteful to Pycnopodia. Further detailed studies of this interaction
would be of value.
It should be stressed that successful escape from the two predators by Tegula
montereyi is dependent upon accurate recognition of its attacker. A deep withdrawal into
its shell would probably not be successful against Pycnopodia (recall that this species
ingests its prey) and exposing its soft parts to tube feet of Pisuster would be equally
inappropriate. Numerous laboratory studies have documented the ability of prey to
distinguish between predators and non-predators (e.g. Edwards, 1969; Phillips, 1976,
1977) and between foraging and non-foraging predators (Dayton et al., 1977; Phillips,
1978). My results for Tegula montereyi indicate that some prey species can also
distinguish between similar predator species and respond differently to each. Whether
this recognition is mediated by water-borne chemicals (e.g. Mackie, 1970; Phillips,
1975), squeaking ossicles (Dayton et al.. 1977), or other mechanisms awaits further
research.
Evidence from field studies support the conclusion that the defenses of T. montereyi
are more effective. When mixed groups of all three Teg-ufu species were tethered in the
kelp forest adjacent to Hopkins Marine Station, T. montereyi was consumed significantly less often than the other two species (over 90% of the mortality was caused by
starfish; Watanabe, in press). Harrold (198 1) found a lower occurrence of T. montereyi
in natural diets of Pisaster in this kelp forest than the other two Teguk species. Tegufa
montereyi also never occurred in the stomachs of 41 Pycnopodiu sampled during a
year-long study in this kelp forest; Tegula pulligo and T. brunnea occurred fairly
frequently (T. Hen-linger, pers. comm.).
Although T. montereyi possesses the most effective anti-starfish defenses of the three
Teg&, the morphological data show that it may be the most susceptible species to
268
JAMESM.WATANABE
crushing predators. Further work on the effects of crushing predators on these species
is needed. However, it seems clear that a prey species cannot be equally well defended
against all of its predators, especially if those predators are functionally diverse (e.g.
extractors such as starfish or crushers such as crabs and fish; see Vermeij, 1978;
Lubchenco & Gaines, 1981; Menge & Lubchenco, 1981 for further discussion).
The large literature dealing with escape behaviors and defense mechanisms of prey
(see Feder & Christensen, 1966; Ansell, 1969; Mackie & Grant, 1974 for reviews)
attests to the common occurrence and diversity of such responses in nature. Behavioral
responses similar to those described herein have been found in a number of other
gastropods in the family Trochidae. Avoidance, flight, shell-twisting, and dropping-off
are common responses of trochids (and species in other families as well) to starfish and
predatory gastropods (e.g. Bullock, 1953; Clark, 1958; Feder, 1963; Hoffman &
Weldon, 1978; Fawcett, 1979; Schmitt, 1981; Harrold, 1982). The morphological
defense of Tegulu montereyi against Pisastergiganteus (i.e. its larger shell size) also occurs
among small Tegulufunebralis (Markowitz, 1980). To my knowledge, apparent distastefulness similar to that of T. montereyi has not been documented for any other trochid,
although the keyhole limpet, Diodora aspera (Margolin, 1964), cowries (Cypraeidae;
Thompson, 1969), and various opisthobranchs (e.g. Thompson, 1960; Paine, 1963;
Ambrose et al., 1979) may employ such defenses.
Defenses that have been described for other trochids that are not present among the
three species examined in this study include an aggressive biting response by Calliostoma
ligutum (Harrolti; 1982) and indigestibility. In a study of Tegula aureotincta and T. eiseni
in southern California, Schmitt (1981, 1982) found that T. eiseni was significantly harder
to digest than the other species and that this difference was correlated with a lower rate
of predation on T. eiseni.
A wide diversity of defensive adaptations against the same predator species can be
found among closely related, sympatric prey (Schmitt, 198 1; this study). Investigations
of factors leading to the evolution of such contrasting adaptations among ecologically
similar species will be a fruitful area for future research in predator-prey relationships.
Documentation of defensive adaptations of prey in the laboratory is a necessary first
step to understanding predator-prey interactions. However, knowledge of how these
relationships operate in nature is necessary before factors selecting for various adaptations in evolving predator-prey relationships can be understood.
ACKNOWLEDGEMENTS
This paper is a portion of a dissertation submitted in partial fulfillment of the
requirements for the Ph.D. in the Department of Zoology, University of California,
Berkeley. I thank the following persons: Drs. W. Sousa, R. Caldwell, R. Colwell,
C. Hickman, D. Phillips, S. Levings. C. Baxter, C. Harrold, and L. West provided
valuable input during this project.
Facilities at Hopkins Marine Station were generously made available to me by Dr.
C. Pittendrigh and I wish to thank the entire faculty and staff of the Station.
GASTROPOD
ANTI-PREDATOR
DEFENSES
269
Research support was provided by a Chancellor’s Patent Fund grant from U.C.
Berkeley and a National Science Foundation dissertation grant (OCE79-13418).
Further support was provided by a Regents Fellowship from U.C. Berkeley and a
National Science Foundation Graduate Fellowship.
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