Chapter 7. Homing Behavior of Achatina fulica
Introduction
Many species of Pulmonats are known to show homing behaviors, that is, the same snail returns to the same place repeatedly after going out from that (Limax flavus and Limax maximus: Taylor, 1907; Gelperin, 1974; Limax psudoflavus: Cook, 1979, 1980; Limax grossui: Cook, 1977; Deroceras (= Agriolimax) reticulatum: Nemall, 1966; Rollo et al., 1981; Deroceras caruanae: Rollo et al., 1981 Ariolimax columbianus: Ingram and Adolph, 1943; Rollo et al., 1981; Arion ater; Rollo et al., 1981; Arion circumsriptus: Rollo et al., 1981; Arion hortensis: Rollo et al., 1981; Arion subfuscus: Rollo et al., 1981; Onchidium floridanum; Arey & Crozier, 1921; Onchidium verruculatum McFarlane, 1981; Cepaea nemoralis: Cameron and Williamson, 1977; Rollo et al., 1981; Helix aspersa: Farkas and Shorey, 1976; Helix pomatia, Pollard, 1975; Lind, 1989). The sensory basis for homing in some terrestrial pulmonates has been identified as chemoreception (Edelstam and Palmer, 1950; Gelperin, 1974).
Croll and Chase (1977) showed that Achatina fulica is able to have a long-term memory for food odors. Two groups of A. fulica were fed either cucumbers or carrots for 86 days. Subsequent tests with a Y-maze olfactometer showed that each group preferred the odor of the food that they have eaten as compared to that of another food. It seems that A. fulica has an ability to remember chemical stimuli. However, no study was reported on homing ability of A. fulica. In this study, I verified whether or not A. fulica has a homing ability by means of mark-recapture experiments.
Materials and Methods
1.Study site
The activity pattern of Achatina fulica was observed in a lawnplot isolated from the other habitats by a road and waterway in Chichi-jima. The lawnplot is 2m wide and 10m long (Fig.29). Several hibiscuses plants grown there, and thin litter and dead twigs are accumulated around the roots of these trees.
Since the dead twigs were removed by hand, snails become to rest at the places near the root of hibiscus during day-time. The surface of the lawn was directly exposed to the sunlight, thus snails had never moved out to the lawnplot during daytime in fine days. Snails concentrated near roots during day time. Accordingly, resting sites were restricted to seven points where hibiscus were grown. In the lawnplot, the following two experiment were conducted.
2. Observations on locomotive activity at night
On 10 June 1989, every snail found in the study site was collected, and only subadults and adults (for distinction between these age categories see Chapter 3.) were used as experimental animals. These snails were individually marked with water-proof paint on the last whorls of the shells and then returned to the resting sites where they were collected.
Movements of marked snails were traced at one hour intravels from 6:00 p.m. to 6:00 a.m. and the locations of moved snails were individually recorded and mapped. This experiments was repeated for the following nights, 12, 14, and 16 June, 1989. 3. Snail movements examined by removal and transplanting.
To test the homing ability of A. fulica, seven marked snails were transplanted from their resting sites to that of the other snails in each day from 23 to 31 June, 1989, and their resting places were examined every day.
Results
1. Movement patterns at night.
Snails crawled out from their resting sites to the lawnplot at night. In the rainy day, the same thing was observed even in daytime. They foraged and mated in the lawnplot. In dry weather, they started to move out two or three hours after the sunset and returned to their resting sites several hours before sunrise. Figure 30 shows the movement trails of eleven snails during the study period. This result showed that subadults moved about more actively than adults. Mean distances of movements significantly differs between subadults and adults. In addition, adults returned to the previous resting sites, while subadults changed their resting sites every day.
2. Mark-recapture experiment
Table 5-a and b show the results of observations on the resting sites of 73 individuals during two weeks. Adult snails rarely changed the resting sites, although a few of them changed their resting sites. On the other hand, subadults changed their resting sites almost every day, although a few of them stayed at the same site for two days. Subadults often moved to much more distant sites in a day than the case of adults which changed their resting sites.
In the case of subadults, there was a considerable number of immigrants to experimental plot from outsides, instead of many emigrants. Eleven marked subadults in total left in the plot, but 23 unmarked subadults immigrated from outsides. Eleven of those immigrants finally crowed out from the plot after two weeks. The number of subadults remained in the plot during two weeks was ten, which is equivalent to 47.6% of the initial number of subadults found in the plot.
3. Transplantation of snails
Table 6 shows the result of the transplantation experiment of snails from their resting sites to the other ones. Only adult snails were used for this experiment, because subadults showed a remarkable large mobility. All individuals that were moved to the other sites returned to their initial resting sites during the experiment of five days, except for one case; No.31 stayed in the site where it was moved in. Individuals that were not transferred between sites did not change theie resting sites.
Discussion
1. Homing behavior of Achatina fulica.
The results of the present experiments showed that the adults of A. fulica have a homing ability, while subadults do not show such an ability clearly. It is considered that homing ability of A. fulica seems to be age-dependent. A similar phenomenon has been observed in a slug, Limax pseudoflavus. Rollo and Wellington (1979) reported that an old large slugs showed a strong homing behaviour compared with a young small slugs.
Chase et al. (1980) studied the distribution of juvenile A. fulica in a plastic box and found that they concentrated to certain points of the box. He described that the degree of aggregation depends on the age of animals, their genetic relationship, and the time of the day, since the snail begin to aggregate a few days after hatching. He also described that aggregation is greater among snails from a single egg clutch more than that from two different clutches, and aggregation is also greater at night than in the daytime.
In the case of A. fulica, however, snail gathering in the resting sites can not be considered as aggregation behavior, because they do not aggregate in usual habitats such as forest floor or road-side shrubs. The gathering in the experiment might be due to the limitation of resting sites. However, the results of this experiment indicate that the adults of A. fulica has an ability to return to the same resting sites. This fact strongly suggests that they can home under certain conditions. Aggregation of A. fulica, which was found by Chase et al.(1980), seems to be a charac teristic only in young juvenile stage. 2. Adaptive significance of homing in Pulmonates.
Land snails and slugs seems to have evolved behavioral adaptations to cope with physical and biotic constraints in the terrestrial environment. One of the important problems to face with pulmonates is body-water loss, which strongly affects their survival (Riddle, 1983). This can be partly solved by modulating activities both seasonally and diurnally (Bailey, 1975, 1981) and by making proper use of microhabitats, which function as shelters for them.
In pulmonate, homing under natural conditions has been seldom investigated, because it is difficult to trace their movements. In laboratory, observations have been done on the species of Helicidae and Limacidae (Gelperin, 1974; Pollard, 1975). Recently the behaviors of a few species have been analyzed quantitatively in laboratory and under seminatural conditions (Cook, 1979, 1980; Rollo and Wellington, 1981). Lind (1989) reported that, in Helix pomatia, a long-term memory for homing to hibernating sites lasts for three years. The present study provided the example of homing in A. fulica under natural conditions.
The first detailed report on pulmonate homing is that of Edelstam and Palmer (1950) on H. pomatia. In their study, marked individuals came back to the original shelter from 40m a place. However, the snails were not able to return when they were transplanted to 150m distant place. Their results showed differed in relation to weather and season, with the best performance in the summer.
A similar behavior was observed by Southwick and Southwick (1969) in A. fulica which was able to return when displaced for 5 to 30m from its shelter. However, the animals were transplanted from the resting sites to the open field where they presumably forage. Their study, accordingly, does not indicate whether A. fulica home to the same resting sites repeatedly. The present work showed that adults of A. fulica return by themselves to their original resting sites even after transplanted to the other resting sites. This result strongly indicates that they prefer the old resting sites and return there repeatedly. Rollo and Weillington (1979) and Cook (1981) stressed that the availability of resting place in daytime is a critical factor to matured slugs for returning to shelters after foraging or mating in nighttime. The homing ability varies in the species of slugs. Limax psudoflavus returns to shelter (Cook, 1979), while Ariolimax reticulatum does not to do so (Newall, 1966). Helicella virgata sometimes shows a precise homing (Pomeroy, 1968). A similar case of A. fulica has been reported by Chase et al.(1980).
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3. Orientation mechanisms
Return to former resting sites requires a memory or recognition of chemical trails. Mucus trail-following occurs in pulmonates (Cook, 1977; Chase et al., 1978) and is effective over a long distance, explaining possible homing to resting places in slugs (Gelperin, 1974; Cook, 1979a, 1980). Homing by means of trail-following has also been proved in various aquatic snails (Funke, 1968; Wells & Buckely, 1972; Cook, 1979, McFarlane, 1981). The present results of movement patterns of adults of A. fulica at night do not support the trail-following hypothesis, because they did not crawl along the old trails on the way back to their resting sites (Fig. 2). In some slugs distant detection of home-cues seems to be the only mechanism involved in homing (Gelperin, 1974), while other species may adopt both this mechanism and trail-following (Cook, 1979, 1980). Recent experiments on Limacus flavus (Chelazzi et al., 1988) showed that distant chemoreception dominates over trail-following when the two mechanisms are put into comparison in binary choice tests.
Snails and slugs frequently home to a communal shelter as described earlier. Rollo and Wellington (1981) found that Agriolimax columbianus homes more frequently to an occupied shelter than to currently empty one . Limacus flavus heads toward a communal refuge when it is offered another alternative one, even if both are currently empty (Chelazzi et al., 1988).
Orientation toward conspecifics or chemicals extracted from their pedal glands has been investigated in A. fulica (Chase et.al., 1978; Chase and Boulanger, 1978). Chase et al.(1980) discovered that in A. fulica the chemical cue is kin-specific. It has a great deal of implications of sociobiological interest. All these observations support the hypothesis that one or more pheromones are secreted by the resting snails and used as homing beacons by conspecifics or relatives. It is an important subject to isolate and to identify the pheromone critical for homing from Achatina fulica