Ronald Chase

Tentacular function in snail olfactory orientation

Summary1.The olfactory orienting behavior of the terrestrial snailAchatina fulica was studied in intact animals, in animals with bilateral lesions of either the anterior tentacles or the posterior tentacles, and in animals with unilateral lesions of the posterior tentacles. Tentacular function was evaluated under three different conditions.2.One assay required the snails to locomote upwind in a two-armed olfactometer and enter the side in which the airstream contained a food odor. The performance of intact controls was statistically indistinguishable from that of snails with bilateral anterior tentacle lesions or snails with unilateral lesions of the posterior tentacles. Snails lacking both posterior tentacles performed at chance levels (Table 1).3.The second assay consisted of trail following on a mucus slime trail. Bilateral posterior tentacle amputations were without effect, but bilateral amputations of the anterior tentacles led to a significant deficit compared to intact controls (Table 2).4.The third assay measured the accuracy of locomotion to a distant odor source in still air. A circular arena was employed. Intact snails and snails with bilateral lesions of the anterior tentacles consistently oriented with a high degree of accuracy. Animals with unilateral or bilateral lesions of the posterior tentacles failed to orient. The unilateral amputations produced a turning bias towards the intact side (Fig. 2).5.The results demonstrate thatAchatina can orient to olfactory stimuli by at least three different means, namely, anemotaxis, movement up a concentration gradient and trail following. The anterior and posterior tentacles are involved differentially in these behaviors. Also, anemotaxis requires only a single tentacle (klinotaxis), whereas orientation to concentration gradients utilizes simultaneous bilateral comparisons (tropotaxis) (Table 3).

Dart receipt promotes sperm storage in the garden snail Helix aspersa

Abstract. During courtship, many helicid snails attempt to pierce the body walls of their mating partners with mucus-coated calcareous darts. The mucus covering the dart induces conformational changes in the female reproductive tract of the recipient, closing off the entrance to the gametolytic bursa copulatrix. We have tested the effect of dart receipt on the number of sperm stored by once-mated snails, Helix aspersa. Snails that were hit by darts stored significantly more sperm than did snails that were missed. Additionally, the effect of the dart was stronger in smaller animals and the number of sperm stored decreased with the shell volume of the recipient. Although larger animals produced larger spermatophores, dart-shooting success was not related to the number of sperm transferred. These data suggest a role for dart-shooting in post-copulatory sexual selection.

A long-term memory for food odors in the land snail, Achatina fulica.

Two groups of Achatina fulica were fed either cucumber or carrot for 86 days. When subsequently tested in a Y-maze olfactometer, each group oriented preferentially toward the odor of that food which it had previously eaten. Two separate measures showed that the memory for these odors lasted 120 days. This represents a new form of behavioral plasticity for gastropod molluscs and offers attractive advantages for the study of neuronal mechanisms in learning and memory.

Determinants of paternity in the garden snail Helix aspersa

Abstract. Despite the likely importance of post-copulatory sexual selection in simultaneous hermaphrodites, the factors influencing sperm competition in these organisms are generally unknown. We have investigated the effects of dart-shooting, mating order, and several other predictors on the proportion of offspring fathered by penultimate (Pn-1) and ultimate (Pn) sperm donors in multiply mated garden snails, Helix aspersa. While paternity ratios were biased towards the penultimate donor (mean Pn-1=0.61), the magnitude of this advantage was dependent upon which of the two donors successfully darted the recipient. Mean Pn-values increased from 0.17 when the recipient was hit by the penultimate donor to 0.39 when it was hit by the ultimate donor. Furthermore, the effect of the dart was more pronounced in the clutches of smaller recipients. From these results, and observations of live sperm in the storage organs, we propose a novel mechanism to explain the detected pattern of sperm utilization in helicid snails. Electronic supplementary material to this paper can be obtained by using the Springer LINK server located at http://dx.doi.org/10.1007/s00265-002-0519-6.

Plasticity of olfactory orientation to foods in the snailAchatina fulica

SummarySnails were tested in an olfactometer for their orientation to food odours. Measures of odour choice, latency to make a choice and percentage of upwind orientations were obtained after experimental manipulations of dietary experience and hunger motivation. Juvenile snails, given an exclusive diet of a certain food for 12 h or less, oriented preferentially toward the odour of that food when subsequently presented with a choice between it and a novel food odour (Fig. 2). A 48 h period of exposure to a food resulted in a 21 day retention of the odour preference (Fig. 3). There was no evidence for an especially sensitive period for conditioning during the first 50 days of age (Fig. 4); however, adult snails (minimum 1 year old) required longer periods of dietary exposure to establish equivalent food odour memories (Fig. 5). Measures of latency and percentage of upwind orientations confirmed the choice data in demonstrating an effect of dietary experiences on olfactory orientation. Hunger motivation increased the selection for familiar food odours, and reduced the latency (Fig. 6 and Tables 3 and 4). Sensory adaptation appears inadequate to explain the conditioning phenomenon since formation of the preferences was contingent upon ingestion of the foods; exposure to the food odours alone was insufficient (Table 2). The data suggest that orientation preferences derive from a learned association between the odour of a food and its nutritional value.

Structure and function in the cerebral ganglion

Evidence is reviewed to evaluate whether the term “brain” is justified in referring to the snails cerebral ganglion. The focus of the review is terrestrial species, with particular attention given to the genus Helix. In accordance with a standard definition of “brain,” the cerebral ganglion is found to be differentiated both structurally and functionally. It receives convergent sensory inputs from a variety of anterior sensory organs plus the posterior body wall. Its outputs comprise motor commands directed towards anterior muscle systems, e.g., the tentacles and the penis, as well as premotor commands directed towards executory centers in other ganglia, e.g., the buccal, visceral, and pedal ganglia. Of the three major divisions in the ganglion, the procerebrum and the mesocerebrum are the most differentiated, whereas the metacerebrum is the least differentiated. The specializations of the procerebrum for olfactory functions, and the mesocerebrum for reproductive functions, reflect the importance of adaptations for feeding and mating in the evolution of the Gastropoda. Microsc. Res. Tech. 49:511–520, 2000.

Synaptic glomeruli in the olfactory system of a snail, Achatina fulica

SummaryThe presence of synaptic glomeruli in the olfactory afferent pathway of vertebrates and arthropods is a striking example of neuroanatomical convergence. To test the generality of this analogy, the olfactory receptors in a terrestrial snail, Achatina fulica, were labeled and traced by application of horseradish peroxidase to the epithelial surface at the tip of the posterior tentacles. All afferent fibers enter the digitary extensions of the tentacular ganglion. The majority of fibers travel through the digits to terminate either in the tentacle ganglion per se or in the cerebral ganglion. About 10% of the afferent axons terminate in glomeruli within the digits. The glomeruli are characterized by dense neuropils, numerous synaptic contacts, and enclosure by glia cells and glial processes. Periglomerular interneurons lie in close proximity to the glomeruli. There are about 20 glomeruli per tentacle. They have irregular shapes with a mean individual volume of 38 × 10-5 mm3.

The olfactory sensitivity of snails,Achatina fulica

Summary1.A two-chambered tentacular olfactometer was constructed (Fig. 1). This device permits the local delivery of odors to the tentacular sensory epithelium, with independent control over concentration on the left and right sides. The occurrence of discrete head turns during locomotion, subject to criteria of latency and extent, was indicative of olfactory orientation response.2.Concentration-response profiles were obtained by delivering odors unilaterally (Fig. 8). The snails turned towards the vapors of amyl acetate, hexanoic acid, butyric acid and 2-octanol. The threshold sensitivities (typically, at 10−7 molar concentrations) were at least two orders of magnitude higher than comparable thresholds reported for other animals (Table 3). In contrast to the odors listed above, there were no reliable orientation responses for acetaldehyde, valeraldehyde, trans-2-hexenal or ethanol.3.None of the odors reliably elicited turning away from the stimulus, despite the observation of tentacular retractions associated with some odors at high concentration, indicating aversive stimulation (Fig. 8, Table 2).4.When amyl acetate was delivered at different concentrations to the two tentacles, the difference between the number of turns towards the strong side and towards the weak side increased as a function of the Weber fraction, with 0.75 being the minimum Weber fraction at which the difference was statistically significant (Fig. 9).5.The methodology was relatively insensitive to inter-observer variations (Fig. 4). However, some factors which did affect the results in particular experiments were age of the snails (Fig. 5), hunger motivation (Figs. 6 and 7) and order of stimulus presentation (Fig. 6).

Chemotactic behaviour inOctopus

Summary1.Small octopuses,Octopus vulgaris, (150 g) were blinded by section of the optic nerves to eliminate the use of visual cues. The animals were placed in a transparent Plexiglas tube (9 cm × 60 cm) that was continuously perfused with fresh sea water, and their behaviour was observed following the introduction of single organic compounds at known concentrations (Fig. 1).2.Alterations in the ventilation rhythm (puffing) were elicited by glutamic acid 10−4 mol/l, glycine 10−4 mol/l and adenosine 5′-monophosphate (AMP) 10−7 mol/l. Arm waving and the forced expulsion of water through the siphon (blowing) were also observed with the same stimuli. Sea water controls showed significantly lower rates of response (Fig. 2).3.Locomotion was elicited by glutamic acid 10−4 mol/l, glycine 10−3 mol/l, and AMP 10−6 mol/l (Fig. 2). The direction of locomotion was invariably upstream (51 trials). Because the stimuli were introduced to either the right or the left of a partition which bisected the upper third of the experimental tube, it was possible to evaluate the animals perception of stimulus location. Two criteria were used: the entry of an animal into the space at either side of the partition, and the initial distribution of an animals probing arms on the two sides (Table 2). In both cases, the results indicate an orientation towards the stimulus source, i.e. chemotaxis.4.The frequency of responding, for all types of response, decreased from the first to the last trial in each testing session (Fig. 3). Sensitization was demonstrated by giving theOctopus a small piece of fish between stimulus trials (Fig. 4).5.The suckers on the arms of theOctopus are believed to be the sensory structures responsible for the observed behaviours. The chemical sense may be an important adjunct to vision in the search for food under natural conditions.

Comparative morphology of three types of projection-identified pyramidal neurons in the superficial layers of cat visual cortex.

The morphology and dendritic organization of corticocortical neurons in the superficial layers of area 18 that project to area 17 were studied by intracellular injection of lucifer yellow in the fixed‐slice preparation. This corticocortical population contains primarily standard pyramidal cells, but occasional nonpyramidal, modified, fusiform, star, and inverted pyramidal cells were also seen. All cell types were present throughout layer 2 and in the upper and middle parts of layer 3. Standard pyramidal cells were found exclusively in lower layer 3. The mean somatic area of the area 17 projecting neurons was 251 μm2. The width of basal dendritic fields was correlated to cell size for standard pyramidal cells but not for the other cell types.