Shell-less Nucella lamellosa (Gmelin) from the rocky intertidal zone of San Juan Island, Washington.

ABSTRACT In the summer of 2004, seven Nucella lamellosa snails from the rocky intertidal zone were found to have detached from their shells after collection. The snails continued to live and function normally for several weeks after discovery. The loss of the shell may have been a reaction to stressful environmental stimuli.

KEY WORDS: gastropod, shell loss, defense, behavior

INTRODUCTION

Shells in gastropods primarily serve as a means of defense against predation. Shell ornamentation, an increase in shell size or thickness, and complex apertural morphology may have evolved in response to changes in the type and strength of predation (Vermeij 1977). For marine gastropods, the shell is the first and often the last line of defense. Other marine organisms use automatization, or the purposeful losing of a body part, as a means of defense through distraction. Hermit crabs will often "give up" a limb when handled roughly (Bertness 1981, Robinson et al. 1970). These and other crab species readily regrow lost limbs. This type of defense is also found in vertebrate species, such as geckos and lizards, which will automatize their tails to distract a predator, enabling a quick getaway (Arnold 1988, Congdon et al. 1974). This paper reports a case of potential nonlethal shell automatization in a marine gastropod species under stressful circumstances.

Background

Nucella lamellosa (Gmelin 1791) is an intertidal, predatory gastropod (family Muricidae) that ranges along the Pacific coast of North America. Nucella kill and consume their prey by either drilling through the shell or wedging open the prey item's shell margin with their apertural edge (Barnett 1979, Perry 1987). They can be found throughout the bays and lagoons of San Juan Island, which is located in Puget Sound in the Pacific Northwest of the United States.

MATERIALS AND METHODS

During the summer (July to August) of 2004, several hundred N. lamellosa specimens were collected from multiple locations throughout San Juan Island. The snails were collected from Argyle Creek (a tidally influenced creek), and False Bay (a tidally flooded and exposed bay). They were collected by hand at low tide and placed into 10-gallon plastic buckets filled with seawater from the location. The N. lamellosa were then transported back to Friday Harbor Laboratories and kept in a tank that received a constant input of seawater.

Several specimens of N. lamellosa were observed to lose their shells under captive conditions (Fig. 1A). The snails would be found "naked," clinging to a surface, with an empty shell nearby in the tank or bucket. The first "naked" snail was rapidly consumed by crabs that were kept in the same tank, so all future specimens were maintained in an isolation chamber. The "naked" snails were offered mussels and barnacles for food. This paper describes the conditions under which the "naked" snails were found and discusses possible reasons for the loss of the shells.

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"Naked" Snail Observations

Several collections of intertidal taxa were made to provide specimens for other studies not reported herein. During one of the initial collections made at Argyle Creek, a single specimen of Nucella lamellosa was found clinging to the bottom of the transport container, without a shell (7.19.04). This was presumed to be an accident, and the snail was placed in a collection tank and eaten by crabs. A week later (7.26.04), another shellless gastropod was collected from Argyle Creek. This specimen was placed in an isolation chamber in a tank of normal N. lamellosa. The other snails in the isolation tank did not appear to respond differently to the "naked" individual. The "naked" snail displayed behavior similar to that of the normal snails, including climbing up the sides of the tank and aggregating with the other snails in corners. A week later, the "naked" snail successfully drilled and consumed a mussel.

During a laboratory experiment taking place in a water table, a third snail was found without its shell. The spigot to this table had become blocked by detritus, and water flow had been very weak to nonexistent for several hours. The snail was allowed to continue in the experiment and consumed three barnacles after it had lost its shell. This implies that the apertural wedge strategy is not necessary for barnacle predation by N. lamellosa.

During a large collection of N. lamellosa at Argyle Creek the next week (8.9.04), three individuals were found shell-less, whereas a fourth was found extruding partway out of its shell (Fig. 1B). The partially detached specimen was found completely separated from its shell several hours later. These snails were all placed into an isolation chamber in the N. lamellosa tank and offered barnacle-encrusted rocks. These snails remained alive, undamaged, and fully functional for two weeks. The dropped shells that were located were undamaged and had no visible tissue attached. The attachment site for the columnar muscle was not examined, so the absence of tissue at the attachment site cannot be confirmed.

The snails come out of their shells with a dark orange color to their flesh, visible veins, and coiled bodies. As time passes, the color lightens to off-white, and the veins become less prominent (Fig. 1C). This may be because of light breaking down the pigment in the newly exposed tissues. The snails also increase in girth, and their bodies become less and less coiled. This may be bloating caused by absorption of seawater through mantle tissue that is normally not exposed, or the expansion of the mantle cavity after the confining pressure of the shell has been removed.

It must be emphasized that at least two of the "naked" snails were observed to successfully kill and consume the normal prey species of N. lamellosa (mussels and barnacles). In both cases, the snails and their prey were isolated from other possible predators, and boreholes were observed on the shells of the prey. This indicates that the loss of a shell does not prevent the successful acquisition and consumption of prey by N. lamellosa.

Other Reports

There have been very few reports of gastropod shell automatization in the literature. Read (1965, 1966) reported four shellless specimens of Littorina littorea (family Littorinidae) in the eelgrass beds of The Salt Pond in Bluehill, ME. The animals were undamaged, with normal, attached opercula and no visible shell.

Hartog (1988) observed that three female Epitonium clathratulum (family Epitoniidae) were found detached, or capable of being easily removed from their shells, after oviposition and just prior to an epidemic die-off. The loss of shell in a live animal has also been observed in Nucella ostrina (Rich Palmer, personal communication).

DISCUSSION

Several reasons have been offered for the apparent ability of snails to detach from their shells unharmed. Read (1965, 1966) hypothesized that the gastropods were either shell-less mutants, or weakened by disease or parasites so they could be easily pulled out of their own shells. The gastropods observed by Hartog (1988) dropped their shells just prior to a postreproductive die-off. He hypothesized that they were weakened by reproduction, and the weight of the shell was enough to cause it to detach from the animal.

The N. lamellosa in the present study were subject to stress during the collection procedure, including low flow, light and oxygen conditions, changes in temperature, as well as overcrowding and proximity to predators. The snail in the flow tank was exposed to similar conditions during the time the water flow to the tank was restricted. The "naked" snails continued to live, feed, and function for weeks after automatization, indicating that the loss of the shell was not a result of disease or weakness. No physical damage was observed on any of the snails. Only seven out of several hundred N. lamellosa were observed to have dropped their shells, indicating that this is probably not a widespread phenomenon. The loss of shell also leaves the gastropods very vulnerable to predation, making this phenomenon unsurvivable in natural settings.

Gastropods have a defensive response behavior that involves the lifting of the shell and violent contortions, which swing the shell from side to side. Buccinum undatum exhibited this behavior in the presence of sea stars, which allowed them to quickly detach from the substrate and escape (Harvey et al. 1987). Limpets also violently twist their shells, and the sharp edge of the aperture can function as a slashing weapon (Hughes 1986). Land snails violently twist their shells in response to physical stimuli (personal observation). In this study, individual N. lamellosa were observed to abruptly twist their shells while crawling on several occasions, although the proximate reason for the twisting was not apparent. It is possible that the N. lamellosa observed in this study detached from their shells during this type of violent contraction and contortion, in response to adverse stimuli, such as crowding or proximity to predators.

It is proposed that this undue stress may have caused some N. lamellosa to drop their shells. It may be that a small proportion of the population has a weakened columnar muscle attachment, and normal escape or stress-induced behavior may cause the shell to become detached. Also, as the first shell-less gastropod was rapidly consumed by a crab, it would be highly unlikely that this trait offers any sort of advantage to snails in the wild.

CONCLUSION

A small proportion of N. lamellosa collected from the rocky intertidal of San Juan Island were found to be capable of losing their shells without any physical damage. These "naked" snails continued to locomote and feed normally for several weeks after shell loss, with only a slight increase in size and change of color. This probably does not represent a case of "deliberate" automatization, as seen in crabs and lizards. This case of "naked" snails leaves open the intriguing possibility that automatization is possible in marine gastropods, and may be related to other defense behaviors.

ACKNOWLEDGMENTS

The author thanks M. Kowalewski, L. Leighton, R. Plotnick, G. Vermeij, and the reviewer for advice and commentary on the manuscript. She would also like to thank S. Koy and Friday Harbor Laboratories for providing funds in support of her research.

LITERATURE CITED

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Hartog, J. C. 1988. An unusual phenomenon observed in Epitonium clathratulum (Kanmacher, 1797) (Prosobranchia: Epitoniidae): live snails becoming separated from their shells. Basteria 52:3-7.

Harvey, C., F. Garneau & J. H. Himmelman. 1987. Chemodetection of the predatory sea star Leptasterias polaris by the whelk Buceinum undatum. Mar. Ecol. Prog. Ser. 40:79-86.

Hughes, R. N. 1986. A functional biology of marine gastropods. Baltimore, MD: Johns Hopkins University Press.

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Vermeij, G. J. 1977. The Mesozoic marine revolution: evidence from snails, predators and grazers. Paleobiology 3:245-258.

KAREN KOY

University of Illinois at Chicago, Chicago, Illinois

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