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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. 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