Pacific Science (1980), vol. 34, no. 3 © 1981 by The University Press of Hawaii. All rights reserved

Defensive Responses of Marine Gastropods (Prosobranchia, ) to Certain Predatory Seastars and the Dire Whelk, Searlesia dira (Reeve)!

DANIEL L. HOFFMAN 2

ABSTRACT: Qualitative comparisons of the predator-induced defensive be­ haviors of four of trochid gastropod, Margarites pupil/us, M. sal­ moneus, M. rhodia, and ligatum, under controlled laboratory conditions indicate that the degree and strength of the response varies according to the sensory information received from a predator and according to the species of predatory seastar or gastropod inducing the response. Generally, all four species of gastropod demonstrate a weak to moderate avoidance response to the scent of such predatory seastars as hexactis and ; whereas direct contact with their soft parts elicits strong and often violent defensive behaviors characterized by shell twisting, propodial rearing which often leads to a loss of contact with the substrate, and somersaulting by metapodial thrusting. It is hypothesized that the inversion of the shell induced by direct contact with a predator sets up the metapodial thrusting behavior and also part of the righting repertoire, which facilitates more rapid flight from the predator. Margarites spp. respond to the scent and contact with the dire whelk, Searlesia dira; whereas Cal/iostoma is unresponsive to the snail, but more responsive to the scent and contact of the sunstar Pycnopodia helianthoides than are the other species of gastropods studied.

THE ABILITY OF AN to interpret var­ sensory cues used to elicit the response and ious sensory cues within its environment the complexity of the response; even the age concerning the proximity of a predator has and size of the snail affect the response major survival value. Phillips (1978) has (Hoffman and Weldon 1978, Phillips 1978). pointed out that certain marine , Presently, there is a wealth of information such as the purple sea urchin Strongylocen­ attesting to the role of chemicals from var­ trotus purpuratus, are able to distinguish be­ ious seastars which trigger a wide range of tween inactive and actively foraging pre­ defensive responses in a number of marine datory seastars. Also of significance from a (Feder and Christensen 1966, cost basis, is the intensity of the response by Feder 1972). Certain other sensory moda­ the animal to the actual or potential threat lities might also be involved; for example, of . An example of such a cost Dayton et al. (1977) have suggested that involved in a defensive response would be some marine animals may respond to vi­ the loss of purchase with the substrate, in­ brations caused by the ossciles of seastars creasing the likelihood for an intertidal rubbing together as the animals move. animal to be dislodged by wave action and While in residence at the Friday Harbor killed. Defensive responses of closely related Laboratories during the spring of 1978, I species of trochid gastropods differ in the had the opportunity to study the defensive behaviors of several species of intertidal and subtidal gastropods (superfamily: Tro­ 1 Manuscript accepted 25 November 1979. 2Bucknell University, Department of Biology, Lewis­ chacea): Margarites pupil/us (Gould, 1849), burg, Pennsylvania 17837. the puppet margarite; M. salmoneus 233 234 PACIFIC SCIENCE, Volume 34, July 1980

(Carpenter, 1864), the salmon margarite; M. species from northern California north. rhodia (Dall, 1920), the rosey margarite; and Margarites rhodia (M. inflata Carpenter, (Gould, 1849), the west­ 1864) is a subtidal species that ranges from ern ribbed topshell. Schroeter (1972) has Prince William Sound, Alaska, to Crescent shown that M. pupil/us responds defensively City, California. Although it would be to a wide range of predators. difficult to determine whether Schroeter Also, Weldon (1977) has demonstrated an (1972) was studying both M. pupil/us and M. avoidance response of C. ligatum to pre­ salmoneus, he found populations of Mar­ datory seastars. Moreover, for comparative garites at Cantilever Point to be primarily purposes, defensive responses have been doc­ subtidal. The distribution of the population, umented in many trochid genera, such as size, and recruitment were found to be (Bullock 1953, Feder 1963, Yarnell closely related to the abundance of the algal 1964, Weldon 1977, Holfman and Weldon canopy (Laminaria spp., primarily). 1978), Cal/iostoma (Feder 1967, Ansell 1969, appear to be their primary food source, and Weldon 1977, Weldon and Holfman 1979), Schroeter notes that the algal canopy may (Feder 1967), Cittarium (Holfman increase concentration and thus in­ and Weldon 1978), (Clark 1958), fluence population growth. Sexually mature Norrisia (Bullock 1953), and (Clark snails live for at least 2 years, and may live 1958, Kohn and Waters 1966). for as many as 4 years. The present paper reports on observations and Pisaster ochra­ of the defensive responses of four species of ceus are common forcipulate seastars in trochid gastropods when presented with dif­ the rocky intertidal region of the west coast ferent species of predatory seastars and the of North America (Ricketts and Calvin dire whelk, Searlesia dira (Reeve, 1946). It is 1962). In the San Juan Islands of Washing­ hoped that these observations may help ton State the vertical range of these two characterize trophic relationships that exist species is +1.5 to -0.9 m; the foraging within this particular low intertidal-subtidal activities of both species are characteristi­ community, as well as present more infor­ cally highest in the summer and lowest in the mation on the variety of predator-induced winter (Mauzey 1966, Paine 1966, Menge responses of trochid gastropods. 1972b). They are food generalists, eating , , , , and snails (Mauzey 1966, Paine 1966, Mauzey, Birkeland, and Dayton 1968, Menge 1972b). NATURAL HISTORY There is strong evidence that in certain inter­ The populations of two species of Mar­ tidal areas of San Juan Island they are also garites, M. pupil/us and M. salmoneus, along important predators of species of Margarites with populations of Calliostoma ligatum, (Menge 1972a). Pycnopodia helianthoides, appear to be sympatric in their distribution. one of the largest of seastars, reaching dia­ The M. salmoneus has a type locality of meters in excess of 1.3 m, occurs subtidally Monterey and is usually considered to be a on mud, sand, shell, gravel, and rocky bot­ southern subspecies of pupil/us. Abbott toms as well as the lower rocky intertidal, (1974) records M. pupil/us as having a distri­ but in protected waters it seldom occurs in bution from the Bering Sea to San Diego, the intertidal (Mauzey et al. 1968). In the California, and he describes it as being a San Juan Islands the diet of Pycnopodia common littoral species in the northern half consists primarily of clams, especially of its range. Margarites salmoneus ranges Saxidomus; and there is evidence that it will from Washington to southern California and feed on urchins, and to some extent crabs, is uncommonly found in 12-80 m of water. holothurians and snails (Mauzey et al. 1968). According to Abbott (1974), C. ligatum The buccinid gastropod Searlesia dira is typ­ ranges from Alaska to San Diego, Cali­ ically found on major combinations of all fornia, and is also a very common littoral substrates, with the exception of sand, and Defensive Responses of Marine Gastropods-HoFFMAN 235 has a vertical range within the intertidal termine the effect of predators on prey from + 1.7 to - 1.8 m (Louda 1979). Sear­ species in a still-water environment (a tidal lesia was long thought to be a scavenger but pool situation), 9-12 specimens of the same is now described as an active carnivore that trochid species were placed in a glass bowl preys on barnacles, limpets, chitons, and (top diameter either 11.5 or 20 cm) that was snails (Louda 1979). Pisaster ochraceus and half filled with seawater. After an accli­ Leptasterias hexactis, along with Searlesia mation period of 10 min, either a predator dira, were all collected a few decimeters or a 20-ml aliquot of seawater that con­ below mean low water at Cantilever Point. tained the predator's "scent" was slowly Small specimens of Pycnopodia helianthoides added to the bowl. The aliquots were taken (average diameter 30 cm) were collected from a beaker that had held one predator either by dredging or scuba diving. per given volume of seawater (100 ml per Leptasterias and Searlesia, 750 ml per Pisaster and Pycnopodia). The control for this experiment entailed adding a similar MATERIALS AND METHODS volume of SBawater taken from an intake The gastropods and used in valve. All bowl experiments were run be­ this study were collected in the intertidal and tween 08: 00 and 11: 00 PST under the sub­ subtidal waters of San Juan Island, Wash­ dued lighting conditions of the laboratory. ington, during the months of March and A Plexiglas V-shaped olfactometer (ap­ April 1978. With the exception ofMargarites proximately 90 x 20 x 14 cm) was used to rhodia, which was dredged off a shell-soft test the ability of the gastropods to detect mud substratum in approximately 10 m of the waterborne scent of a potential predator. water off the main dock of the Friday Presumably, if the scent is detected, the gas­ Harbor Laboratories, the remaining three tropods will increase the rate of locomotion species of trochid gastropods were collected and distribute themselves in the device at a a few decimeters below mean low water of distance from the source of the stimulus. the rocky intertidal off Cantilever Point This experiment is based on those under­ (40 0 30'29"N, 123°0'3"W). taken by Phillips (1975, 1976). The V-shaped All animals were maintained in 11 0-185­ olfactometer was positioned on a seawater liter Plexiglas aquariums that were supplied table with the branched arms facing a with running seawater (temperature approxi­ window with a northern exposure. Reser­ mately 8-110C). The seastars and predatory voirs at both ends of the olfactometer were gastropods were maintained in aquariums supplied with running seawater from the separate from the trochid gastropods used in intake seawater system; the water was then this study. Generally, the animals were al­ allowed to run down the main chamber. lowed to acclimate to the laboratory con­ Predators were placed within one of the ditions for 3 days before studies were under­ reservoirs so that the water would flow over taken. Every 2 weeks new snails were col­ them before passing through the perforated lected to prevent the habituation that might partition and down the side branch. The result from snails being tested repeatedly. number of predators placed in each reservoir Behavioral observations were made under was a function of their size, since a large two different experimental conditions: still predator produces more scent than a much water in a glass bowl and flowing water smaller predator and the snail would then within a Y-shaped olfactometer. The experi­ respond much more to the larger specimen ments were designed to test the ability of than to the smaller one (Phillips 1976). To various predators to elicit defensive be­ compensate for a possible size effect, six haviors from certain species of trochid gas­ Leptasterias (average diameter 5.5 cm) and tropods either through contact or distance one Pisaster (diameter 12.7 cm) were con­ chemoreception and to characterize the re­ sidered to be of equivalent volume in this sponses elicited by the prey species. To de- series of experiments. The other reservoir of TABLE I

SCENT- AND CONTACT-INDUCED RESPONSES IN THREE SPECIES OF Margarites AND Calliostoma ligatum WITHIN THE CONFINES OF WATER-FILLED GLASS BOWLS

PREDATOR

Leptasterias he_"wetis Pisaster oehraeeus Pyenopodia helianthoides Searlesia dira PREY SPECIES (n = 12) (n = 8) (n = 4) (n = 8)

M. pupillus (n = 128) } Scent: A, B Scent: A Scent: little or no response Scent: A, B, E M. salmoneus (n = 114) Contact: C, D, E, F, G Contact: C, D, E, F, G Contact: C, D Contact: C, D, E, H M. rhodia (n = 54) Scent: A Scent: A Scent: little or no response Not tested Contact: C, D, E, F, G Contact: C, D, E, F, G Contact: C, D Not tested C. ligatum (n = 120) Scent: A, B Scent: little or no response Scent: A, B, E Scent: no response Contact: C, D, E, F, G, H Contact: C, D, E, F, G, H Contact: C, D, F, G Contact: no response

NOTE: A, extension and waving of cephalic and epipodial tentacles; B, heightened crawling movements; C. contraction of head and tentacles; D, rearing and rapid retreat; E, shell twisting; F, loss of purchase with substrate (especially with prolonged contact); G, leaping and somersaulting with the metapodium; H, movement upward and out of the water; n, total number of snails and seastars observed. Defensive Responses of Marine Gastropods-HoFFMAN 237

the olfactometer held no predator and for instance, the adherence of podia to the served as a control. Twenty-five to seventy­ shell. This shell-twisting behavior, which has eight specimens of trochid gastropods (de­ been reported in many trochid genera pending on the species tested) were closely (Ansell 1969), may have adaptive value in grouped in the main chamber of the Y­ extricating the snail from the grasp of the shaped olfactometer. After 2-4 h, the po­ predator (Hoffman and Weldon 1978). sitions of the snails within the two side Similar shell twisting has been observed in branches and the main chamber of the olfac­ Margarites pupil/us when conspecifics at­ tometer were recorded. Controls were made tempt to graze on algae growing on in total darkness (with the device enveloped another's shell (Schroeter 1972); however, in in an opaque plastic tarp) and also in the this case, the grazing-induced response is not light with the absence of any predators. followed by any rapid flight movement. These latter experiments tested whether light Prolonged or repeated contact with a pred­ would affect the distribution of the gas­ ator sets up a propodial rearing response tropods within the olfactometer. that usually results in loss of purchase with the substrate and an overturned shell. Under normal circumstances, in the absence ofpred­ ators, inverted snails invariably right them­ RESULTS selves with a propodial pull. However, in Descriptive data of the predator-induced Margarites and Calliostoma, if the propo­ responses of three species of Margarites and dium cannot make contact with the sub­ Calliostoma ligatum are summarized in strate, the elongated posterior end of the Table 1. For the most part, the responses of foot or metapodium folds along its long axis these snails are consistent and quite similar. and thrusts its pointed tip into the substrate. The basic differences between the two genera The foot thrust causes the shell to rotate, relate to the degree of responsiveness to facilitating propodial contact with the sub­ different predatory species. For instance, strate and thus righting. However, predator­ Margarites spp. show little or no response induced overturnings greatly exaggerate the to the scent of Pycnopodia helianthoides; metapodial thrusting behavior, especially whereas a moderate flight response is elicited with repeated contact stimulation by a pred­ in Calliostoma by the seastar. Also, two ator (Weldon and Hoffman 1979). The snails species of Margarites respond moderately to relinquish their foothold and roll the shell the scent of Searlesia dira and very strongly over repeatedly by swinging their foot to contact with the soft parts of the snail; against the substrate (Figure 1). This leaping however, Searlesia elicits no avoidance re­ or somersaulting response has been des­ sponse from Calliostoma. cribed in several species of Calliostoma The difference in stimulation between (Feder 1967, Ansell 1969, Weldon 1977, waterborne scents and contact with the pred­ Weldon and Hoffman 1979). The thrusting ator is one of intensity. The scent of pred­ escape maneuvers on a smooth hard sub­ ators increases the activity of the snails, strate such as a flat rock or glass aquarium eliciting an extension and vigorous waving tend to be somewhat exaggerated in that the of the cephalic and epipodial tentacles and smooth top-shaped shell has more of a ten­ an increase in the ditaxic locomotory gait. dency to roll; in fact, such surfaces make The contact stimulus always surpasses the righting more difficult. But, on irregular or threshold intensity of distance chemorecep­ rough surfaces, such as gravel or algal mats, tion, with the rearing of the anterior end of inverted shells have less tendency to roll, the foot or propodium and an abrupt change facilitating not only escape but also righting. in the direction of movement, often by as Predator-activated snails show an in­ much as 120°. The shell is often twisted creased negative geotaxis (movement through an arc of 180°, espedally if pro­ upward) on submerged vertical surfaces. longed contact is made with the predator, Generally, Margarites stop at the air-water 238 PACIFIC SCIENCE, Volume 34, July 1980

FIGURE I. Sequence of two metapodiaI thrusts by M argariles pupillus to contact with Leplaslerias hexaclis over a period of 5 sec. A, metapodium fully extended in a thrust position; B, shell flips, making contact with , metapodium upward at end of thrust; C, initiation of second thrust movement with metapodium in contact with substrate; D, fully extended metapodium flips snail away from the starfish.

interface, often protruding the head out of scent of a predator borne in flowing water is water. Once they initiate movement, they presented in Table 2. In the absence of a may crawl just beneath the surface, often predator, and under both lighted and dark with the edge of the shell out of water. conditions, Margarites pupil/us tends to dis­ Searlesia is able to elicit a response from tribute itself randomly within the confines of Margarites strong enough to stimulate a V-shaped olfactometer after 2-4 hr. movement completely out of the water. However, with the introduction of a pred­ Calliostoma, on the other hand, usually ator to the system, the movements of the crawls completely from the water when snails result in a distribution that is signif­ direct contact has been made with either icantly nonrandom, i.e., significantly greater Leptasterias or Pisaster. Water evacuation than expected from a 50: 50 distribution (X 2 induced by predators has been observed in > 3.8, p < 0.05). It appears that M. sal­ the trochid Tegula funebralis (Feder 1963). moneus and Calliostoma ligatum are more Such species as Acmaea limatula and able to differentiate the scent of Pisaster than A. scutum also show a negative geotaxis on is M. pupil/us. submerged vertical surfaces to predator Although Pisaster and Pycnopodia cap­ scent; this tends to move them out of the tured and initiated feeding responses on foraging range of predators (Phillips 1976). Margarites and Calliostoma within glass Data on the ability of a snail to detect the bowls, neither Leptasterias nor Searlesia Defensive Responses of Marine Gastropods-HoFFMAN 239

TABLE 2

RESPONSES OF Margarites AND Calliostoma TO THE SCENT OF PREDATORS IN FLOWING WATERS OF AN OLFACTOMETER

NUMBER OF SNAILS TO

MIGRATE TO MIGRATE TO CHAMBER REMAIN IN EXPERIMENTAL CHAMBER WITH WITHOUT ORIGINAL PREY SPECIES n PREDATOR n CONDITIONS PREDATOR PREDATOR CHAMBER

M.pupillus 148 Light 33 36 79 150 Dark 31 37 82 185 Leptasterias 18 Light 21 75 89 105 Leptasterias 12 Dark 11 29 65 119 Pisaster 2 Light 31 34 54 112 Searlesia 11 Light 28 36 48 M. salmoneus 58 Leptasterias 12 Light 7 34 17 61 Pisaster 2 Light 3 32 26 C. ligatum 40 Leptasterias 6 Light 4 18 17 40 Pisaster I Light 5 18 19

NOTE: The test criterion for a positive response was an unequal distribution of snails within the two branches. Chi-square values resulted from comparing numbers in the two branches by means ofa 2 x 2 contingency table (X' > 3.8, P < 0.05). demonstrated any feeding behavior under ingly, the complexity of responsiveness ap­ similar circumstances. Additional feeding­ pears to be related to the strength of the preference experiments were performed in stimuli eliciting the responses. Also, the de­ the laboratory using a covered 8-liter plastic fensive responses of these two genera for the aquarium supplied with running seawater. In most part are quite similar to each other. one experiment, 4 Leptasterias (average dia­ The differences between them primarily are meter 6.0 cm) were placed in the aquarium in their responsiveness to different predatory with 24 M. pupillus and 24 C. ligatum. After seastars or gastropods. Unlike the strong 36 hr, 4 Margarites had been eaten. Under scent-induced avoidance responses of Tegula similar conditions, 6 Searlesia were placed in funebralis (Feder 1963) and juvenile Cit­ the aquarium with 24 M. pupillus and 24 tarium pica (Hoffman and Weldon 1978), for Trichotropis cancellata, a subtidal mesogas­ the most part Margarites and Calliostoma tropod. No snails were attacked or eaten show fairly weak to moderate avoidance after 36 hr. However, I was able to observe responses to such waterborne scents. It is two Searlesia actively feeding on M. pupillus only through direct contact with the soft below the zero tide mark of Cantilever Point parts of these predators that strong, and during the low tide period, 24 April 1978. often violent, defenses are evidenced. If the scent or odor alone elicits an avoid­ ance response, as it does in certain trochid genera, does the resultant response direct the DISCUSSION snail away from the grasp of the predator? The predator-induced defensive responses From the experiments with waterborne of M argarites ahd Calliostoma observed in scents in an olfactometer, the question ap­ the laboratory are similar to those described pears to be answered in the affirmative. for other genera of trochids studied both Although these data do appear to be signif­ under artificial and field conditions (Bullock icant, it would be difficult to extrapolate 1953, Clark 1958, Feder 1963, Yarnell 1964, these laboratory conditions with those of the Feder 1967, Ansell 1969, Weldon 1977, marine benthos, especially in such micro­ Hoffman and Weldon 1978). Not surpris- habitats as the undersurfaces of marine 240 PACIFIC SCIENCE, Volume 34, July 1980 where the hydrodynamics are considerably sponses of Fasciolaria (Wells 1970, Snyder more complex. The fact that Margarites and and Snyder 1971) and Strombus (Berg 1974, Calliostoma are able to show some, albeit at Field 1977), where the digs into times a weak, response to the scents of the substrate and flips the shell from the various predators is of significance to their predator. survival. Perhaps, as Phillips (1978) clearly The similarity of foot movements involved demonstrates, these gastropods may be able in the righting and defensive behaviors of to differentiate more readily between forag­ some gastropods has been well documented ing and nonforaging predators. During the (for a review of the literature, see Weldon course of the experiments within the olfacto­ and Hoffman 1979). Gore (1966) and Gonor meters, only Leptasterias of those predators (1966) suggest that gastropods that have tested showed any activity by moving about developed a kick or thrust mode of righting the chamber, and all three species of snails have coupled these movements secondarily tested did respond positively to the scent of with defense. Given the similarity of these this seastar. It also may be difficult for snails movements, the hypothesis that kick and to determine the direction from which the thrust righting historically precede these predator's scent is emanating, especially in movements is quite reasonable. An alterna­ still waters. Kohn and Waters (1966) ob­ tive hypothesis has been proposed by Weldon served that Trochus pyramis would actually and Hoffman (1979) that kick and thrust crawl toward textile, turning quickly movements evolved primarily in escape and before directly encountering them. Mar­ appear secondarily in righting. If one as­ garites also crawls over the shell of Searlesia, sumes that the propodial pull was the primi­ only to react strongly after contacting the tive mode employed by gastropods in soft parts of the predator. righting-and all modern species of gas­ M argarites and Calliostoma have evolved tropods with the exception of such limpetlike a series of interrelated behavioral responses genera as Acmaea, Crepidula, and Fissurella that are initiated by direct contact with a are able to demonstrate this ability (Weldon predator; these are (1) propodial rearing that 1977, Weldon and Hoffman 1979)-then a often results in a loss of purchase with the modification of a predator-induced thrusting substrate, with the snail being overturned, and somersaulting behavior of such genera and (2) thrusting with the metapodium that as Margarites and Calliostoma may have results in somersaulting. Propodial rearing is served to orient the shell when the pro­ of special significance, as Feder (1963: 508) podium had difficulty in contacting a surface described for a predator-induced reaction in to right upon. Perron (1978) presents evi­ Tegula brunnea, "the heavier turban shell dence on this ontogeny of the escape re­ tends to throw the animal off balance when­ sponse in the primitive strombid Aporrhais ever the foot is raised, and the gastropod occidentalis; that is, the foot leap used in falls off its rocky substrate." Similarly in locomotion may have first appeared as part Calliostoma and Margarites, propodial rear­ of an escape response to slow-moving ing sets up the conditions that make a more predators. rapid egress possible. In the inverted state It is possible to speculate that the kick and the metapodium is able to function as a thrust foot movements are often, but not muscular lever that, by repeated thrusts always, triggered by contact with a predator. against the substrate, flips the shell from the Gore (1966) observes the kicking and shell­ immediate vicinity of the predator through a twisting response in Nassarius when direct series of violent somersaults. Such predator­ contact is made with the seastar Luidia. induced foot thrust movements have been Also, Field (1977: 2) reports that the kicking well documented in Nassarius (Weber 1924, escape response in Strombus macultatus is 1926, Gore 1966), and should not be con­ "triggered usually either by some movement fused with the predator-induced kick re- of the Conus or by direct contact." In ad- Defensive Responses of Marine Gastropods-HoFFMAN 241 dition, the mushrooming response of limpets components of the diets of these predatory is elicited by contact with echinoderms seastars and snails. (Bullock 1953). In those species of gas­ tropods that demonstrate strong avoidance responses to predators through distance ACKNOWLEDGMENTS chemoreception, such as Tegula funebralis (Feder 1963, Yarnell 1964) and Cittarium I would like to acknowledge the facilities pica (Hoffman and Weldon 1978), there is no and cordialities afforded me by A. O. D. evidence of any complex kicking or thrusting Willows, Director of the Friday Harbor behavior. For both these species there is no Laboratories. I also extend thanks to Robert evidence of predator-induced loss of contact L. Fernald, David King, Craig Young, and with the substrate, because the basic strategy Alan Murray, for their help in collecting is accelerated locomotion away from the snails; to Joseph Rosewater of The U.S. source of stimulation. Of interest is the National Museum, and James H. McLean, brown turban snail, Tegula brunnea, of Curator of Malacology of the Los Angeles which Feder (1963) notes a tendency to be County Museum of Natural History, for easily overturned when stimulated by a pre­ identifying several species of gastropods. dator. Although no foot thrusting or kicking And many thanks are in order to Paul J. has ever been described, Weldon (1977) has Weldon for kindly providing very useful observed that unlike its congener, T. fune­ criticisms of the manuscript. bralis, the inverted T. brunnea will not only probe with its propodium but can probe and right itself with the metapodium as well. But LITERATURE CITED in this case the tip of the metapodium func­ tions more as an organ of prehension, and ABBOTT, R. T. 1974. American . 2d not, as in the case of Calliostoma, as a lever. ed. Van Nostrand Reinhold, New York. The negative geotactic response on ver­ ANSELL, A. D. 1969. Defensive adaptations tical surfaces of Calliostoma ligatum may be to predation in the . Symp. Mar. an adaptation to their environment. McLean BioI. Assoc. India, II. 487-512. (1962) has found this species to be most BERG, C. J., JR. 1974. A comparative etholog­ abundant on submerged walls near the kelp ical study of strombid gastropods. Behav­ beds off the central California coast. iour 51 :274-322. Encountering a predator would tend to BULLOCK, T. H. 1953. Predator recognition move the snails upward, or in the case of and escape responses of some intertidal direct or prolonged contact, would result in gastropods in the presence of starfish. a loss of contact with the vertical surface and Behaviour 5: 130-140. an all or nothing escape to the bottom; CLARK, W. C. 1958. Escape responses of whether such an action would ultimately herbivorous gastropods when stimulated be conducive to survival has yet to be by carnivorous gastropods. Nature, determined. London 181: 137-138. . Finally, there is good field evidence that DAYTON, P. K., R. J. ROSENTHAL, L. C. the predators that elicit defensive responses MAHEN, and T. ANTEZANA. 1977. in M argarites and Calliostoma do feed on Population structure and foraging biology them under natural conditions, even though of the predaceous Chilean asteroid they may not comprise a major part of their M eyenaster gelatinosus and the escape diet (Mauzey et al. 1968, Menge I972b, biology of its prey. Mar. BioI. Louda 1979). The behavioral defenses of 39:361-370. these gastropods may reduce predatory pres­ FEDER, H. M. 1963. Gastropod defense re­ sures on their populations and in doing so sponses and their effect in reducing pred­ effectively serve to reduce their role as major ation by . Ecology 44: 505-512. 242 PACIFIC SCIENCE, Volume 34, July 1980

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:e F $$5#5 i "14!.i&¥%fii!i#- s. p! p,,. 4 At .i&S4* 52 ,w'm!3El9!'P@?!4I'!"..,tVM0'. ¥S¥ Defensive Responses of Marine Gastropods-HoFFMAN 243

WELLS, F. E. 1970. An ecological study of YARNELL, J. L. 1964. The responses of Tegula two sympatric species of Fascialaria Junebralis to starfishes and predatory (Mollusca: Gastropoda) in Alligator snails (Mollusca: Gastropoda). Veliger Harbor, Florida. Veliger 13 :95-108. (SuppI.) 56-58.