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An Experimental Analysis of the Escape Response of the Gastropod

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An Experimental Analysis of the Escape Response of the Gastropod Pacific Science(1977), Vol. 31, No.1, p. 1-11 Printed in Great Britain An Experimental Analysis of the Escape Response of the Gastropod Strombus maculatus I LAURENCE H. FIELD 2 ABSTRACT: The escape response of Strombus maculatus is described in detail, including the apparent adaptive morphology of the foot, operculum, and eyestalks. The response is elicited by a chemical stimulus from two molluscivorous species of Conus and two gastropod-eating species of Cymatium but not from other pre­ datory species of these genera. Strombus habituated within three trials to a solution of "factor" from Conus pennaceus, but habituated only rarely, and then only after many trials, to contact with the live Conus. It was concluded that the eyes of S. maculatus are not used to see the Conus; however, eye removal significantly disrupted the orientation of the escape response, suggesting that the animal monitors some environmental cue such as polarized light. Tentacle removal appeared to interfere with escape response orientation but only to a variable extent. HERBIVOROUS GASTROPODS exhibit distinctive posterior end of the foot is thrust against the escape behavior from sea stars (Bauer 1913, substrate, causing the shell and head to lunge Feder and Christensen 1966) and predatory forward. Little additional work has been done gastropods (reviews by Kohn 1961, Robertson on strombid locomotion, and as Kohn and 1961, Kahn and Waters 1966, Gonor 1965, Waters (1966: 341) indicated, "the component 1966). 'Strombus has the remarkable ability to steps of the process have not been analyzed and escape from predators by rapid lunges, using the the functional morphology remains to be operculum to push against the substrate (Kohn studied in detail." Recently Berg (1972) and Waters 1966). Gonor (1966: 227) described described the ontogeny of several strombid b~­ the response of S. gibberullls and S. luhuanus to havioral patterns, including locomotion. In Aulica vespertilio and Conus marmoreus. Both addition, Berg (1974) made a subsequeilt species of Strombus escaped by "moving away analysis, based on the present report, .of with quick kicks of the foot until they were behavior patterns in 10 species of Indo-Pacific about 30 cm away". Kohn and Waters (1966) strombid gastropods. analyzed quantitatively the escape response of I studied escape behavior of the Hawaiian S. canarium to C. textile: the animal "leaped" species Strombus maculatus Sowerby, which approximately 16 mm every 1.6 sec; at a mean reacts to the presence of gastropod predators, rate of progression of 6.8 mm/sec. In these particularly Conus pennaceus. This response species ofStrombus, escape behavior differs from differs from those described previously for normal locomotion only in its much accelerated Strombus in that S. macula/us actually propels pace. N ormallocomotion has been described by itself backward, clear of the substrate, travelirig Parker (1922) as "leaping," in which the up to 2.5 times its shell length, activity never observed during normal locomotion (described briefly below). I This research was supported by United States National Science Foundation grant no. GB-6134. This paper describes the escape response in Hawaii Institute ofMarine Biology contribution no. 496. precise terms and discusses the associated adap­ Manuscript accepted 10 November 1975. tive morphology. Locomotory rates were ana­ 2 University of Hawaii, Hawaii Institute of Marine lyzed cinematographically for comparison with Biology, Kaneohe, Hawaii. Present address: University of Canterbury, Department of Zoology, Christchurch 1, Kohn's work. Experimental studies investiga­ New Zealand. ted: (1) the natureofthestimulus and conditions 1 I-2 2 PACIFIC SCIENCE, Volume 31, January 1977 that elicit the response, (2) the attenuation was attached to the bottom with a coat ofresin, of the response to repeated stimuli, and (3) the and concentric circles, 2.5 cm apart, were means by which Strombus receives the stimulus marked on the sand and numbered from the and orients the response during escape from center outward. A Strombus was placed in the C. pennaceus. The attenuation of a gastropod center circle, and escape was elicited by holding escape response was studied briefly by Margolin a live Conus next to it. The number of the circle (1964). He found, as did Feder (1948, cited in in which the animal landed after each jump was Bullock 1953) and Feder (1963), that the dictated into a tape recorder. Sixty-five escape response eventually ceases after the animal has sequences were analyzed from three animals. been"sensitized" to the stimuli. RESULTS METHODS Description ofResponse The 12 Strombus maculatus used in this study (size range 1.7-3.4 cm) were collected on sand Normal feeding of Strombus maculatus con­ and algae-covered intertidal benches around sists of slow ciliary gliding with periodic Oahu, Hawaii. Six were fully grown and six shifting of the shell forward (in contrast to were subadults (outer lip of shell not yet Parker's (1922) description of "leaping") thickened). The animals were maintained in a while the proboscis works back and forth, shaded outdoor seawater table with a sand grazing on minute algae on the substrate. When bottom and fresh, circulated, unaerated sea­ Conus pennaceus is detected within 5 to 10 em, water. Habituation experiments were carried Strombus stops both locomotion and feeding and out in a similar seawater table (67 x 94 cm). partially withdraws into, and lowers, the shell. Motion pictures were made at 16 frames per sec The eyestalk tentacles, which normally extend with a Bolex H-16 camera (16 mm). forward and wave in small arcs, are directed Conus and other reef-dwelling mollusci­ toward the Conus and increase their rate of vorous gastropods were tested by being placed waving, as judged subjectively. The onset of near Strombus. Parts of Conus pennaceus and the escape is triggered usually either by some move­ water in which tne predator had been living ment of the Conus or by direct contact. The were introduced to see whether they would Strombus then pushes quickly against the sub­ elicit the escape response. strate with the posterior part of the foot, pro­ Two types of experiments concerned attenu­ pelling itself backward and slightly to the left. ation ofescape: a Strombus was stimulated every This small initial movement causes the aperture 5 min by (1) contact with a live C. pennaceus, and to face upward or to the side after the animal has (2) by 20 cc of seawater containing a chemical landed. The foot then flexes forward and down, factor produced by C. pennaceus (hereafter its posterior tip flattened against the operculum, referred to as "Conus factor "). A "standard" which is dug into the substrate beneath the shell factor solution was obtained by allowing three (Figure 1A2). Next, the foot violently straight­ to four C. pennaceus to remain in 1 liter of un­ ens, causing a backward flight above the sub­ aerated seawater at ambient temperature for strate for several centimeters (Figure 1A3-A7). 2 hr. In both sets of experiments, the response During the entire response, the proboscis and was recorded in terms oflatency and numbers of eyestalks are extended. The sequence of jumps following each stimulus presentation. Figure 1A is repeated until the animal has I studied the orientation of the response by removed itself from the Conus. After the final making eyestalk and tentacle ablations on jump, the animal rapidly swings the proboscis animals that had been narcotized in 7.5 percent back and forth across the substrate, secures a MgCI2, diluted 2: 1 with seawater. On the day grip with the foot, shifts the shell dorsad, and following an operation, at which time the moves with its normal pedal locomotion, operated animals appeared normal and respon­ testing the environment with the proboscis. At sive, experiments were conducted in seawaterin this point the animal either burrows into the a shallow tray, 1 m2 in area and 8 cm deep. Sand sand or glides away. Escape Response of Strombus maculatus-FIELD 3 5 4 3 2 5cm 9 8 7 6 B c operculum O.5cm FIGURE 1. A, An escape jump ofStrombus maculatus, drawn from consecutive motion picture frames; note use of operculum. B, View of S. maculatus withdrawn into the shell, exposing only the operculum. This illustrates the operculum's serrated edge and small size as compared to the length of the aperture and shell. C, Eyestalks and tentacles of S. maculatus, shown during feeding. The extended proboscis and anterior end of the foot are also seen protruding from the shell. The tentacles may be withdrawn or extended beyond the length illustrated. Escape varied among individuals and from foot and is serrated along its right edge. The day to day in a single individual. Jumps varied serrations seem to grip the substrate efficiently from 2-63 per sequence, with an average as the animal jumps, instead ofcreating a cutting (N = 25) for a Strombus 2.9 cm in length of edge for a defensive weapon, as suggested by 19 (range 5-36). This agrees well with a mean Charles (1966). The operculum appears more value of 18 jumps per response (N = 16) sub­ importantfor its use in the escape response than sequently recorded by Berg (1974) for the same for its typical function in other gastropods species. On one occasion a Strombus did not (closing of the aperture), for the animal rarely jump but instead glided away from a Conus. withdraws into its shell as a protective reaction; instead, it usually makes the escape response. Only the most intense stimuli (e.g., continuous Functional Morphology prodding with a pin) cause the snail to cease the The operculum of Strombus maculatus is escape response and withdraw into the shell. highly modified to form a hard, pointed pivot The foot of strombids is striking in several from which the animal can gain leverage to respects.
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