Observations on the Escape Response in Nassarius Vibex (Say), (Mollusca: Gastropoda) 1

OBSERVATIONS ON THE ESCAPE RESPONSE IN NASSARIUS VIBEX (SAY), (MOLLUSCA: GASTROPODA) 1

ROBERT H. GORE Institute of Marine Science, University of Miami

ABSTRACT Observations were made on the escape response of Nassarius vibex. This reaction, consisting of a violent flipping movement, is used by the snail whenever certain predatory sea stars or molluscs make contact with it. Contact situations involving the gastropods Fascialaria tulipa, F. hunteria, and the sea star Luidia alternata with N. vibex elicited the reaction and were investigated. The escape response is discussed and a possible relationship between righting behavior and escape response is suggested.

INTRODUCTION The escape reaction that is known to occur in prosobranch snails of the genus Nassarius commonly found in the intertidal region, has received particular, though infrequent mention in the literature. Tryon (1882) makes first brief mention of this reaction when he states simply that some "Nassas" spring up and throw themselves over when disturbed. Bauer (1913) reported more completely on this reaction with N assa (=N assarius) reticuLata, and described the flipping reaction as a series of somersaults when the snail was stimulated on the metapodial tentacles by the sea star Astropecten bispinosus. Weber (1924; in Carthy, 1958) illustrated the movement of N. mutabilis as a twisting, side-to-side forward leap instead of a somersault. Hoffman (1930; in Kohn, 1961) said that this response can be induced when the sea star is some distance away, but Bauer (1913) held that contact between sea star and snail was necessary. All three authors agree that contact with the tube feet of asteroids would elicit this response in the snail. Hoffman (1930; in Kohn, 1961) also found that picric acid or chloroform, among other chemicals, similarly elicited an escape reaction in Nassa reticuLata. The escape reaction of molluscs that encounter predatory sea stars or predatory molluscs has been documented by Bullock (1953), Margolin (1964 a, b), Clark (1958), Peters (1964), and Gonor (1965). Gonor described a predator-prey relationship involving Nassarius Luteostoma and its predator Natica chemnitzii. A comparison in the literature of N. Luteostoma, N. reticuLata, and N. mutabilis shows that the escape response is somewhat similar in all three species. It differs only in whether the snail somersaults or leaps diagonally forward.

'Contribution No. 692 from the Institute of Marine Science, University of Miami. 424 Bulletin of Marine Science [16(3) I observed that Nassarius vibex also utilizes an escape reaction when it is stimulated by either the sea star Luidia alternata Say or by the gastropods Fascio/aria hunteria Perry or F. tulipa Linnaeus. This reaction consists of continual thrusts by the foot, which is stretched out until it is very thin. The foot then is used as a lever to push the snail over in a series of somersaults. The foot swings from side to side as the snail somersaults. This results in a violent flipping motion. These observations, and others in the literature, suggest that the somersault or flipping response is a definite escape mechanism used by Nassarius vibex when it is stimulated by potential predators. The purpose of this paper is to report on investigations of both the stimuli and reactions associated with the escape reaction. In addition, a possible relationship between escape and righting behavior is suggested. I am indebted to Drs. Warren Wisby and Arthur Myrberg, and Mr. William Herrnkind, who offered many valuable suggestions and critically read the manuscript. In addition, I gratefully acknowledge the criticisms of Drs. F. M. Bayer and H. B. Moore. Their help was very much appreciated.

MATERIALS AND METHODS Experiments were carried out in flowing seawater on a water table and in two 75-liter aquaria. The aquaria were filled with 4 em of sand to allow the snails to burrow. Fluorescent lights were located about 3 m over the tanks and table. Each tank held approximately 300 N. vibex from 5 to 15 mm long. Tests consisted of repeated introduction of various sea stars and molluscs, as well as body fluids from these animals, in the immediate vicinity of N. vibex. Any reactions by Nassarius to sea stars or snails were noted. Table 1 summarizes the results together with reactions noted to other animals presented to Nassarius outside the test situation.

REACTIONS TO TEST ANIMALS Individuals of three species of sea star were placed singly into each tank and the water table consecutively in order to observe the flight response of N. vibex to these animals. Repeated introduction of the sea stars resulted in the varied reactions seen. When a 12-cm specimen of Echinaster sentus (Say) was introduced there was no flipping response. This sea star moved slowly compared with Nassarius. The only response noted in the snails throughout repeated introduction was that Nassarius moved from the sea star's path as it approached. Often this sea star would crawl directly over Nassarius, but in most cases, the snails avoided contact. A 14-cm specimen of Astropecten duplicatus Gray also elicited little response. This sea star moved more rapidly than Echinaster, but in only 1966] Gore: Escape Response in Nassarius vibex 425 TABLE] REACTION OF Nassarius vibex TO CONTACT WITH 8 SPECIES OF ANIMALS COLLECTED FROM VARIOUS AREAS IN SOUTH FLORIDA Modeof Reaction Animaltested Placecollected feeding elicited1 Placetested Luidia alternata intertidal carnivore 3,2 Lab & field Astropecten alligator 200 fathoms carnivore ],2,3 Lab A. duplicatus intertidal carnivore 1,2 Lab & field Echinaster sentus fringe reef carmvore 1,2 Lab Fasciolaria tulipa intertidal carnivore 3,2 Lab & field F. hunteria intertidal carmvore 3,2 Lab Natica canrena sub-littoral carnIvore 2,3 Lab Strombus gigas sub-littoral herbivore 1 Lab

'The reaction elicited most is listed first. 1= wilhdrawal inlo shell 2 == active avoidance 3 = flip response two instances was there actual contact between the snails and Astropecten. In both instances the snail bumped into the stationary sea star and then jerked away with a partial somersault. This response may have resulted from contact with the numerous spines along the arm of the sea star. At times, Astropecten also crawled over Nassarius but the snail showed no escape response. A 10-cm specimen of Luidia alternata elicited considerable response. As soon as it had settled to the bottom it began to move rapidly across the sand. Snails which were buried in a resting position emerged immediately before the path of the sea star; usually as soon as the tentacles of the animal touched the extended siphons of the snails. Some snails emerged, however, as soon as Luidia touched bottom. Most Nassarius, if touched on the propodium or siphonal area with tentacles, or, especially the tube feet of Luidia, immediately began violent flipping movements. A few snails simply moved rapidly without flipping from out of the sea star's path or fled before it. But these latter, when touched by tube feet or tentacles of Luidia, would immediately make the flipping response, often turning over five to ten times before righting. Less often they would turn right or left and move rapidly away from the sea star. The gastropod's siphon would be held high and waved over the shell throughout these encounters. Some snails that flipped did so directly into the sea star's path and were overrun. Luidia never stopped when this happened but continued to move quickly across the sand and around the tank. Snails trapped under the arms either continued the flipping action or withdrew deeply into their shells until after the asteroid had passed. Sea stars that touched the posterior of the foot of N. vibex, especially in the region of the metapodial tentacles, rarely elicited a flipping response. The snail seldom varied its direction when stimulated in this manner. The flipping response in N. vibex appeared to be evoked most whenever a 426 Bulletin of Marine Science [16(3) tentacle or, more often a tube foot, of Luidia came in contact with the frontal region of the snaiL This was easily seen in those snails which, in their movement from the sand, emerged directly in front of the sea star and touched its arms. The flipping response was then quick and violent, taking the snail 25 to 30 em away from Luidia. Nassarius then righted itself and continued moving in a normal manner. Wells (1958) has determined that the predacious neogastropod Fascio- laria hunteria will feed on N. vibex to some extent. I have also seen Fascio- laria tulipa feed on Nassarius both in the field and in the laboratory. Each of these species was introduced into the Nassarius tank with similar results. F. tulipa, when either dropped into the water or set quietly on the tank bottom, caused immediate emergence of all Nassarius in its vicinity. They heaved up out of the sand, began exploratory movements with the siphon and moved away from Fasciolaria. There were some Nassarius that moved towards Fasciolaria, or because they emerged near Fascialaria, moved closely parallel with it. When these individuals made contact with Fascialaria with their siphon or propodial tentacle, immediate flipping occurred. The somersaulting response was especially pronounced when the siphon or the ventral surface of the foot of Fascialaria touched any soft part of Nassarius. Fifteen minutes after the fasciolarid snail was introduced, the tank walls became covered with Nassarius as they moved upward to congregate at the water surface. This, and the fact that emergence of N. vibex occurred first in the area where Fascialaria had settled and then at the opposite end of the tank shortly thereafter, implies a good chemosensory ability in N. vibex to detect "odors" carried by water current.

REACTIONS TO ANIMAL FLUIDS I observed that Nassarius would often flip in a section of the tank or water table where no Fascialaria was present. These sections were previously occupied by Fascialaria either as a burrowing site or resting site. When a wooden probe was moved over the sand surface, the particles would cling to the stick in long streamers, indicating a slime trail. Nassarius placed in this area immediately after a fasciolarid had been removed somersaulted as soon as they moved onto this patch. The response could be elicited in different snails for periods of two to ten minutes after the removal of Fasciolaria. The response then diminished and could not be evoked again in every case. If a streamer of slime was wound around a probe and applied to Nassarius in or near the head region, the flipping response could be elicited almost every time. This reaction was also induced by a slime streamer on a wooden probe if the nassarid was touched on any portion of the foot. Tests using only a plain wooden probe merely caused the animal to withdraw into its shell. 1966] Gore: Escape Response in Nassal'ius vibex 427 A 7.S-cm wide trough was set up on the water table. Seawater was piped into one end, creating a current flow that could be varied in speed with the spigot. When Fasciolaria tulipa was placed in the trough downstream from several N. vibex the nassarids always oriented upstream and moved very positively against the current flow, no matter what the current speed. The same fasciolarid placed upstream 1 to 20 cm ahead of the nassarids caused them to cease their forward motion and turn sideways or completely reverse their forward direction. The definitive movement in this response in each instance varied both with the distance between the two gastropods and the individual Nassarius. Only one Nassarius out of 40 tested consistently approached the Fasciolaria. Encountering the fasciolarid it either moved up the sides of the trough and around the predator or stopped and waved its siphon back and forth. When it touched Fasciolaria flipping always took place. Therefore, it appears that a flipping response occurs in Nassarius not only when it comes into contact with the siphon or ventraL surface of the foot but also with slime from Fasciolaria. Furthermore, excised outer sections 3.5 mm long of the lateral surface of Fasciolaria foot caused no response whereas excised portions of the ventral surface of the foot (of the same length) caused flipping in 25 out of 30 snails. Two snails simply turned away and three showed no reaction but withdrawal into the shell when contact was made.

ORIENTATION TO PREDATOR FLUIDS Pieces of filter paper (Curtin No. 7760) were soaked in fluid from either crushed Dca pugilator, Luidia altemata, or Fasciolaria tulipa. Two test situations were devised. In one, the test papers were placed singly in the center of an arena formed by a polyethylene container 35 cm in diameter and 16.5 cm deep. The snails were allowed, one at a time, to orient from the perimeter of the arena, toward or away from the test paper in the center. In the second situation, papers were placed at 900 angles from each other around the perimeter of the arena, with the snails allowed to orient from the center of the arena toward or away from the papers. I suspected that any snail crossing a test paper impregnated with fluid from Fasciolaria or Luidia would show a flipping or avoidance response. Figure la, b, c, d is a diagram of the results of these tests. Ten different snails were used individually in a series of ten tests. In the S-minute testing period per snail (Fig. 1a) every snail oriented to the Dca paper in the center of the arena, regardless of its original starting position at the perimeter. This suggests a klinotactic orientation (Fraenkel & Gunn, 1940) dependent on the chemosensory mechanism in Nassarius. This is an indirect orientation by interruption of regularly alternating lateral deviations with comparison of intensity of stimuli, in this case 428 Bulletin of Marine Science [16(3)

E FIGURE 1. Chemosensory reactions in Nassarius vibex to filter paper soaked with fluids from various animals. Reaction to: (A) Uca pugilator; (B) Luidia alternata; (C) Uc:a surrounded by Luidia; (D) Fasciolaria; (E) Cyprinodon variegatus, Fasciolaria tulipa, Uca pugilator, and a blank; (F) The control situation, no stimuli present. Ten snails were released in all situations but only the results of five are shown to avoid confusion. 1966] Gore: Escape Response in Nassarius vibex 429 through the use of the animal's siphon. The orientation is complex and is probably due to unequal diffusion of Uca juices from the filter paper. This may explain why some snails oriented along the side of the arena before finally turning inward toward the paper. The final directional movements were almost always in a straight line directly toward the source. If the cross marks on each traced path are counted (each mark equal to 30 seconds) an orthokinetic reaction is seen as the snail approaches the source. In this reaction the speed of the snail's locomotion is dependent on stimuli intensity. The snails definitely avoided paper soaked in Luidia juice (Fig. 1b). Four snails moved onto the paper but immediately moved off again. No flipping was seen. The same lighting conditions were present in both Uca and Luidia tests and thus lighting does not appear to influence the observed orientation. When a paper soaked in Uca fluid is surrounded by papers soaked in Luidia fluid (Fig. Ie) chemotactic orientation is again exhibited by Nassarius. The straight line orthokinesis seen with Uca alone is very probably altered by the Luidia papers. At any rate, the Luidia papers are avoided and orientation and movement occur toward the Dca paper. The snails never came close enough to touch the paper soaked in Fascia/aria fluid (Fig. ld). Again, no flipping was observed. Although three snails out of ten moved toward the Fascia/aria paper, they turned from it when they were about 10-20 mm away. These movements would seem to constitute a rather obvious avoidance response. Since the snails would not approach a paper soaked in Fascia/aria fluid no test involving a "goal" paper (i.e., soaked in Dca fluid) surrounded by Fascia/aria-fluid papers was undertaken. Instead, two "attractant" papers soaked with juice from Dca and from the fish Cyprinadon variegatus were placed at opposite sides of the arena. The snails also would orient toward a paper soaked with Cyprinadan and this set-up gave them a choice of goals toward which to orient. In addition, one "avoidance" paper soaked with Fascia/aria fluid was placed at right angles to the two attractant papers. Finally, a blank filter paper was placed in the fourth corner. The negative orientation to both the Fascia/aria and the blank paper, and the positive orientation via chemotaxis to the attractants is easily seen in Figure Ie and needs no comment. Figure If is a diagram of the control situation. No food or predator stimuli were present. Each test consisted of the individual release of 10 Nassarius from the center or from selected points around the container perimeter. After each release there was apparent random movement over the entire container and no noticeable selection of one spot over another. 430 Bulletin of Marine Science [16(3 )

A B c

D E F

G H

FIGURE 2. The righting response in Nassarius vibex. The flipping response follows the same sequence, except that at (F) the righting motion is carried over causing the snail to return to (A) initiating the sequence of (A) through (F) again and again. 1966] Gore: Escape Response in Nassarius vibex 431

DISCUSSION Many genera of sea stars, including Astropeeten and Luidia, will prey on small snails. And it has generally been accepted that some genera of sea stars win cause an escape reflex in certain snails (Clark, 1958; Bullock, 1953). Bauer (1913) in reporting an attack by Astropeeten bispinosus on N. retieulata also mentions an unsuccessful attempt by this sea star to feed on Murex brandaris. The snail's long spines prevented the small, eversible stomach of the sea star from enveloping it. The aspects involving the predator-prey relationships with Nassarius vibex follow along these same lines. Since the Nassariidae are considered to be intertidal gastropods, any predation would be expected to come from predators also found in this zone. Both Astropeeten duplieatus and Luidia alternata are littoral species (see Clark, 1933) found in the same habitat as Nassarius vibex. Yet only Luidia caused a distinct flipping response in my trials; Astropeeten elicited little response from Nassarius. Perhaps Luidia feeds on N. vibex only after the snails metamorphose and while they are still small. The adult snails may be too active for capture. I have found young Nassarius of 2.5 mm shell length in abundance on the mud flats. This size (and possibly up to 4 or 5 mm) might make them easy prey for Luidia and Astropeeten were it not for the escape reflex. In two months of observation on Luidia in an aquarium with about 100 N. vibex of 10 mm shell length or larger, I have never seen the sea star capture a snail, although the snail continues to make the escape response when properly stimulated by the sea star. If given a choice in an aquarium between Nassarius and the cockle Traehy- cardium murieatum, Luidia will ultimately capture the cockle; the cockle also uses its foot to propel itself rapidly across the bottom. Table 1 summarizes the reactions of Nassarius to animals. The data suggest that the flight reflex can only be elicited by the soft parts of the predator, viz. tube feet or tentacles of sea stars, as suggested by Bauer (1913). Even the tentacles of Luidia do not always evoke a flipping response when they touch Nassarius. If a section of sea star arm is placed across the path of the snail in a trough only a change of direction results upon contact. This is hard to explain since the sea star arm is living and presumably emits the same "odor" as the entire sea star. On the other hand, the tube feet almost invariably cause some avoidance reaction, either change of direction or flipping, if they make contact with the snail. The flight response of Nassarius when stimulated by other predacious gastropods is less well documented. Gonor (1965) reports the interaction between Natica chemnitzii var. unijaseiata and Nassarius luteostoma. Wells (1958) merely mentions predation by Fasciolaria hunteria. I have observed this for F. tulipa. Not only do both fasciolarids elicit the flip response when they touch Nassarius, but the presence of F. tulipa will cause Nassarius vibex to emerge from the sand, migrate from the area and crawl 432 Bulletin of Marine Science [16(3) up the walls of the aquarium to the water surface. It appears that detection of fasciolarids is due to emitted chemical stimuli which initiate directional changes and avoidance reactions in the prey. The elicitors secm to be located in the siphonal canal and the outer ventral surface of the foot as well as in the slime glands and secretions from these organs in Fascio/aria. Sensory perception of chemical stimuli over long distances ("smell") would therefore seem to play a vital role in the survival of Nassarius in its interaction with Fascio/aria. It always detected the tulip in both quiet and circulating water. But if the fasciolarid was placed downstream it was not sensed; at least no overt reaction occurred. When placed upstream from N. vibex, however, the latter would change its direction of movement. The gross similarity in N. vibex between the flipping reaction when stimulated by a potential predator and the simple righting response when the snail is overturned is striking. Essentially, in the righting response, the foot is extended from the aperture and swung in a complete reverse. The snail thus becomes oriented to the rear of the shell, with the head pointing toward the spire and the posterior portion of the foot pointing toward the anterior of the shell and the siphonal canal. The posterior portion of the foot is then directed downward until it touches the substrate. Once contact is made, the animal moves with a violent muscular motion and swings the shell around so that it is oriented properly with the head again. At the same time, it rights itself by using the foot as a lever to flip shell and all right side up. This sequence is pictured in Figure 2. The righting behavior is seen whenever Nassarius vibex is completely overturned. Individuals only 3 mm long also right themselves in this manner. The snails right themselves the same way if they are in a dry place, such as a table top. But here the righting response is not completed and results in the snail flipping about, much like the escape response. The movement is neither as violent nor as prolonged as it is in the presentation of a sea star or a predacious mollusc. It is not unreasonable to assume that the flipping response mechanism evolved from a simple righting motion, being simply an extension of the latter which may have gained some measure of protection for these snails. Gonor (personal communication) has observed this flight response in a Nassarius reacting to an Australian volute and to hermit crabs in Alaska. In each instance he considers it merely a righting response that has been extended for escape. Whether this reaction, flight response, fiuchtrefiex, etc., is an escape mechanism in the true sense of the word is open to question. It appears that a simple association was made (Bauer, Weber, and others, loco cit.) when observing a predator (such as a sea star) approaching or touching Nassarius and the latter responding by somersaulting or twisting away. It would seem, in the case of N. vibex at least, that the movement is more of 1966] Gore: Escape Response in Nassarius vibex 433 a reaction to an irritant since it is not always seen in response to the presence of a predator and since the snail does not distinguish between the predator or some substance in the exudate from the predator. This suggests that Nassarius has an individual variable threshold for the stimuli that elicit the flip response. The threshold may be determined in part by the presence or nearness of a predator or some substance from it and water currents carrying the chemical irritant. Both function in the stimulation of the receptors that signal the flip response. Finally, this flip response has drawbacks as an escape mechanism in N. vibex since the motion may actually bring the snail into the path of the predator. In experiments with Luidia this occurred a number of times. In contrast, the response to Fasciolaria is more directed and directional. For example, if the siphon of Fascio/aria touches the posterior portion of the foot of Nassarius the snail will flip forward. If the siphon touches the head part of Nassarius, the snail will flip backward.

SUMARIO

OBSERVACIONES EN LA RESPUESTA DE HUlDA EN Nassarius vibex (SAY) (MOLLUSCA: GASTROPODA) Nassarius vibex} gaster6podo comun en la zona de la marea, muestra una reacci6n de huida en presencia de ciertas estrellas de mar 0 de moluscos predatores. Esta reacci6n consiste en una respuesta de golpe ligero 0 de salto mortal, y es provocada por contacto con los animales predatores 0, en el caso de moluscos predatores, por contacto con su secreci6n. En todos los casos mostr6 evasi6n por ambos, la estrella de mar y los moluscos. Ensayos de orientaci6n usando fluidos de Uca pugilator} Cyprinodon variegatus} Luidia alternata y Fasciolaria tulipa demostraron la capacidad de Nassarius vibex para distinguir el fluido del animal predator del fluido del no predator y dirigirse hacia este ultimo, y evitar contacto con el primero. Esta evasi6n, junto con la variable evasi6n y respuestas de hufda mostradas por los animales predatores, sugiere que la respuesta de huida puede ser tomada como una reacci6n a un irritante que esta presente tanto en el exudado como en los mismos predatores. La eficiencia funcional de la reacci6n de huida de los nasaridos es tambien dudosa ya que algunas veces coloca al caracol directamente en el camino del predator. Finalmente parece haber una relaci6n entre la observada respuesta de enderezarse, vista cuando Nassarius es virado, y la respuesta de huida. La ultima parece ser una prolongaci6n del movimiento de enderezarse que resulta en el efecto de saIto mortal. 434 Bulletin of Marine Science [16 (3)

LITERATURE CITED BAUER, VICTOR 1913. Notizen aus einem biologischen laboratorium am Mittelmeer. !. Einige schutzeinrichtungen der meeresschnecken. Int. Rev. Hydro- bioI. Hydrograph., VI Bd: 1913/14: 31-37. BULLOCK, T. H. 1953. Predator recognition and escape responses of some intertidal gastropods in the presence of starfish. Behavior, 5(2): 130-140. CARTHY, J. D. 1958. An introduction to the behaviour of invertebrates. George Allen & Unwin, Ltd., London, xi + 380 pp., 4 pis., 148 figs. CLARK, H. L. 1933. A handbook of the littoral echinoderms of Porto Rico and the other West Indian Islands. Sci. Survey Porto Rico and Virgin lsI. N. Y. Acad. Sci. XV!., pt. 1: 1-147, 7 pis. CLARK, W. C. 1958. Escape responses of herbivorous gastropods when stimulated by carnivorous gastropods. Nature, 181(4602): 137-138. FRAENKEL, G. S. AND D. L. GUNN 1940. The orientation of animals. Clarendon Press, Oxford, 318 pp. GONOR, J. J. 1965. Predator-prey reactions between two marine prosobranch gastropods. Veliger, 7( 4): 228-232. KOHN, A. J. 1961. Chemoreception in gastropod molluscs. Amer. ZooI., 1(2): 291-308. MARGOLIN, A. S. 1964a. The mantle response of Diadora aspera. Animal Behavior, 12(1) : 187-194. 1964b. A running response of Acmaea to sea stars. Ecology, 45(1): 191-193. PETERS, R. S. 1964. Function of the cephalic tentacles III Littorina planaxis Philippi. Veliger, 7(2): 143-148. TRYON, G. W., JR. 1882. Manual of Conchology. IV. Nassidae, etc. G. W. Tryon PubI., Philadelphia, 276 pp., 58 pis. WELLS, H. W. 1958. Predation of pelecypods and gastropods by Fasciolaria hunteria (Perry). Bull. Mar. Sci. Gulf & Carib., 8(2): 152-166.