Behavior of Gastropod Molluscs

TERESA AUDESIRK and GERALD AUDESIRK,     Biology Department, University of Colorado at Denver, Denver, Colorado

Publisher Summary

Molluscan behavior is extremely diverse, encompassing the relatively limited behavioral repertoire of clams and limpets and the intelligent, highly flexible behaviors of the cephalopods. Gastropods and cephalopods dominate as subjects for molluscan neurobiology for contrasting reasons: (1) cephalopods for the mammal-like intricacy of their brains and behavior and (2) gastropods for their relative simplicity and their large and individually identifiable neurons. This chapter discusses gastropod behaviors, especially those of species commonly used in neurobiology. Light plays an important role in the life of molluscs. For terrestrial forms, bright light can signal heat and dryness, while shade may represent desirable damp shelter. Feeding is stimulated by the detection of food stimuli by the rhinophores, oral veil, anterior foot, or mouth area. Gastropod feeding, like that of more complex organisms, is influenced by the interaction of several variables, including hunger, satiation, quality of food, intensity of the feeding chemostimulus, sensory adaptation, and habituation.

I Introduction

A A Neuroethological Perspective on Behavior

II The Senses: Chemoreception and Vision

A Gastropod Chemoreception

B Visually Mediated Behavior

III Feeding

A The Raspers

B The Browsers

C The Hunters

D Modulation of Feeding

IV Locomotion

A Ciliary Locomotion

B Locomotion by Pedal Waves

C Swimming

D Burrowing

V Defensive Behavior

A Withdrawal

B Defensive Secretions

C Escape Locomotion

VI Reproductive Behavior

A Reproduction in Pulmonates

B Opisthobranchs

VII Behavioral Hierarchies

A Opisthobranchs

B Pulmonates

VIII Perspective

References

I Introduction

Molluscan behavior is extremely diverse, encompassing the relatively limited behavioral repertoire of clams and limpets, as well as the intelligent, highly flexible behaviors of the cephalopods. Needless to say, a single chapter, or indeed an entire volume, cannot begin to do justice to the variety of behaviors displayed by members of the phylum Mollusca. Since this volume is devoted primarily to neurobiology, we have chosen to focus our review on those behaviors which have been, or promise to be, suitable for study at the neural level. The study of ethology, or behavior as performed under natural conditions, has much to offer the field of neuroethology. The neurobiological perspective is that behavior is an emergent property of the intricate interconnections of neurons acting under the influences of hormones and neuromodulators. However, from a broader evolutionary perspective, selective pressure to produce particular adaptive behaviors is the force which has molded the nervous system (Pinsker, 1980).

Gastropods and cephalopods dominate as subjects for molluscan neurobiology for contrasting reasons: cephalopods for the mammal-like intricacy of their brains and behavior, and gastropods for their relative simplicity and their large and individually identifiable neurons. Since the cephalopods are covered in a separate chapter (see Boyle, Chapter 1, Volume 9), we will confine our discussion to gastropod behaviors, especially those of species commonly used in neurobiology. Among the gastropods, members of two subclasses, Pulmonata and Opisthobranchia, predominate as subjects for neuroethological studies. Within these, a few genera stand out: the pulmonates Helix, Helisoma, Limax, and Lymnaea and the opisthobranchs Aplysia, Hermissenda, Navanax, Pleurobranchaea, and Tritonia.

Further, another chapter is devoted specifically to “plastic” behaviors, especially learning (Chapter 2), and thus, little mention will be made here about changes in behavior brought about by experience. Finally, we will not discuss homeostatic “internal” behaviors, such as control of respiration, circulation, and digestion, which are covered in other volumes of this series.

A A Neuroethological Perspective on Behavior

Not all behaviors are equally suited for neuroethological analysis. For example, highly flexible behaviors elicited and modified by subtle and often variable external stimuli and internal motivational states are very difficult to analyze at the neural level. The complexity of the behavior would be expected to be reflected in, and indeed to be caused by, highly variable electrophysiological states in the neurons controlling the behavior, making a definitive analysis of which neurons contribute to the behavior, and their mechanisms of action, very difficult. In fact, fluid, “optional” behaviors, such as mating (which is obligatory over an animal’s life cycle but optional at any given time) tend to be difficult to elicit repeatably in the laboratory, particularly under the conditions required for neuronal recording.

Consequently, most neuroethological studies have concerned behaviors which conform to three criteria: reliability, stereotypy, and robustness.

1. Reliability: The first criterion which a behavior must meet is that it can be reliably evoked in all, or nearly all, animals by the application of well-defined stimuli. As an example, many gastropods, such as the nudibranch Tritonia diomedea (Fig. 25), show escape behavior elicited by contact with specific stimuli, including contact with predators or certain noxious substances (Willows et al., 1973). A T. diomedea will perform its escape swim every time it is touched with the tube feet of the predaceous sea star Pycnopodia, with little habituation during repeated presentations (Abraham and Willows, 1971). If desired, the escape-eliciting stimulus can be quantified in terms of the number of tube feet and duration of contact or of the volume and concentration of noxious chemicals.

2. Stereotypy: The simplest behavior to study on the neuronal level is one which is stereotyped, that is, performed in almost exactly the same way every time. Presumably, the neurons controlling such a behavior are all active each time the behavior is performed, and their activity is nearly identical on each repetition. This greatly facilitates identification of participating neurons and their modes of interaction with one another in producing the behavior. The escape swim of T. diomedea again fulfills this criterion very well, with little variability except in number of swim cycles (Abraham and Willows, 1971). The forms of the swim cycles are extremely regular.

3. Robustness: Finally, recording from identifiable neurons of the central nervous system usually requires that the animal be at least partially dissected (but see Pinsker and Eberly, 1982; Parsons et al., 1983). Therefore, to be amenable to neural analysis a behavior must be robust, that is, the animal (or its appropriate parts) must still perform the behavior after dissection to expose the relevant parts of the nervous system. Escape behaviors are particularly stable in this regard. A massively dissected T. diomedea will still swim upon contact with sea star tube feet, salt crystals, or detergents (Audesirk, 1978b; Willows et al., 1973). Indeed, even the isolated nervous system can be stimulated to generate the underlying motor program for swimming (Dorsett et al., 1969).

As the neural analysis of stereotyped behaviors has progressed, an increasing number of investigators have turned to behaviors which ordinarily fulfill these three criteria but which can be modified under appropriate, carefully controlled conditions. In this regard, feeding, locomotion, and withdrawal have thus far proved to be the behaviors of choice. Each of these behaviors, in certain gastropods, has been found to display various degrees of plasticity, including competition with other behaviors, habituation, and both aversive and nonaversive classical conditioning. Behavioral plasticity and the neural mechanisms where known...