C HOMING BEHAVIOR OF THE LIMPET COLLISELLA SCABRA by Freya Sommer Hopkins Marine Station Stanford University Pacific Grove, CA. Direct all proofs and correspondence to: Freya Sommer Hopkins Marine Station Pacific Grove, CA. 93950 Sommer PART I: Homing behavior of small individuals of the limpet Collisella scabra. Introduction A distinctive characteristic of the limpet Collisella scabra is its ability to return to a very specific "home" site after foraging on the rock while awash or submerged. This phenomenon was recently reviewed by BRANCH (1981). Although homing in C. scabra has been studied quite extensively, the exact mechanism is still unknown. Homing behavior in relation to size of the limpet was studied by JESSEE (1968). His results indicated that there was no significant difference between the homing behavior of large C. scabra, greater than 15mm in length, and that of small limpets between 6 and 10mm long. He suggests, however, that individuals smaller than 6mm long do not usually home. HEWATT (1940) had previously suggested that C. scabra less than 14mm in length do not home. The present study was undertaken to determine whether small C. scabra have the ability to home, and whether the homing is a constant occurence. My results show that C. scabra less than Amm long can indeed home, and that there is less rigidity in homing, i.e. a higher rate of home site changing, than shown in a previous study of larger limpets (BRANT, 1950). Materials and methods The C. scabra studied were located on gently sloping granite. between 2 and 3 feet above MLLW, on a protected shore of Mussel Point. Pacific Grove, California. 26 individuals were chosen and measured with calipers. They were grouped into 3 size classes: less than 2mm C Sommer in length (8), 2-3mm (7), and 3-4mm (11). The limpets were marked with a dot of red nail polish on the apex of the shell, and a dot was painted on the granite imm anterior to the shell. Relative positions of the dot and the marked limpet were noted. A number or letter corresponding to each animal was painted on the rock in the vicinity of the "home" site. During 5 consecutive daytime high tides the limpets were observed every hour for 7 hours, and movements away from home were noted. In preliminary observations, no limpet was seen to start and complete a foraging run in under an hour, so it is assumed that all forays made during each high tide were recorded. No observations were made during high tides at night. If a limpet failed to return to the site where it was originally marked, its new location was marked at low tide. Results Of 26 C. scabra, 6 were never seen to forage (Figure 1). These may have moved during one or more night high tides, or they may not have foraged at all during the study. Of the 20 animals which were seen to move, not every one foraged every day. Only the 20 foraging limpets were included in this analysis of homing behavior. The average total distance travelled by an animal in one foray was about 5cm. Homing was defined as returning to the same site that was occupied before the onset of foraging at high tide, and taking up the precise previous orientation. This was determined by alignment of the painted dots and good fit to the substrate, as far as c Sommer discernible by eye. As can be seen from Figure 1, 85% of the limpets which were seen to forage homed back to their original home sites. This analysis does not explain the fate of the 15% which changed home sites, and actually underestimates homing. The 3 limpets changing sites in Figure 1 did actually show homing behavior as indicated in Figure 2, which analyzes homing according to the total number of forays made during each high tide. Levels of homing are diagrammed in Figure 2a, " 1° homing" is homing to the site wherethe limpet was originally marked. "Site changing" is failing to return after foraging to a site to which homing previously occurred. "2° homing" is homing to the site where the limpet was found after failing to return to the original site. "3° homing" is homing to the site where the limpet was found after failing to return to the 2° site. Figure 2b shows that 84.1% of forays resulted in 1° homing, and a total of 10.1% resulted in 2° or 3° homing. No foray ending in site changing was ever followed by another non-homing foray, i.e. there was always at least one instance of homing to the new site. Discussion The results indicate that small individuals of C. scabra can indeed home, although there is a tendency to change home sites. It is possible that the proportion of 1° homers to home site changers is greater than that suggested by this study, since some C. scabra may have moved and homed once or more during the night high tides. For instance, of all 6 non-movers had foraged at night, then the maximum fraction of 1° homers would be 88.5%, rather than the 84.1% Sommer reported. This is still less than the 97.8% homing reported by BRANT (1950) over a 5 day sampling period for larger C. scabra on low rocks. It would be interesting to study growth rates of small C. scabra in relation to home site-changing frequency, to determine whether a limpet retains its home site longer as it gets larger. It may be adaptive for the young limpet to change sites every so often, in the chance of finding the "perfect" home. Other possible reasons for site changing include interference from other organisms. In two cases, a larger, "intruding" C. scabra wasffound on the home site of the small marked limpet which had settled in a spot away from its home site. Even after the intruder had moved away, 2-4 high tides later, the small limpet did not reclaim its site. Home site changing could possibly be the result of environ¬ mental trauma, which might have smaller effect on the limpet as it grows larger. Sommer PART II: Studies on possible mechanisms of homing in the limpet Collisella scabra. Introduction As mentioned in Part I, the exact mechanism of homing in the limpet Collisella scabra is still unknown. JESSEE (1968), and COOK et al. (1969) attempted to prevent homing behavior in C. scabra by scrubbing the rock surface around the home site, and by applying NaoH or HCl, to destroy any chemical trail that may have been laid down by the foraging animal. Homing was reduced, but not eliminated. JESSEE (1968) believes that this signifies some appreciation of the rock topography by the limpet. COOK ( ?) suggests that a reason for the lack of homing prevention could be inefficiency of methods used in attempting to remove a chemical trail. The purpose of this study was to investigate further the possible mechanisms of homing in C. scabra. Materials and methods There were four stages of experiments. First, home site burning was attempted in the field and in the lab. Second, limpets were taken from the field and put on glass in the lab in order to see whether they 1) conformed to their new substrate, and 2) set up home sites on a flat surface totally devoid of topographical information. Third, a similar test was done, using rocks as substrate instead of glass. Finally, a series of home site transplantation experiments was done in the lab, in which quartz home sites were chiselled off rocks and transplanted, together with the resident limpet, to glass or new rock substrates. Sommer For all lab experiments, artificial high and low tides were created in an outdoor sea-table (Figure 3). "Low tide" was brought about by allowing only a small amount of sea water to run into the table, and by placing a short, hollow plug in the drain, so that the water level remained at about 3", and all the experimental limpets were left high and dry. "High tide" was caused by replacing the short plug with a taller one, and turning on "splash" from perforated tubing connected between water nozzles above the sea-table. All test animals were gradually submerged and able to forage. In this manner, the limpets were subjected to two high tides per day, one at about 8 a.m., and the other at about 7 p.m., each of 2-3 hours duration. Results Home site burning experiments. Home site burnings were first carried out in the field. 20 limpets, 1-1.8cm in length, were selected on one rock face. All were marked as in the small limpet experiments described in Part I. 10 of these were removed from the rock at low tide. A circular area of radius 6-8cm, centered on the limpet's home site, was intensively heated with a propane torch. After the rock had cooled, the limpets were replaced on the rock 8cm from their home sites, aimed tangentially to the treated area, and slightly wetted with sea water to aid in sticking. 10 controls were similarly removed and replaced, on non¬ torched areas. Results are shown in Table 1. By the second high tide after treatment of the limpets, there did not appear to be any difference in the behavior of the two groups of animals. The controls fared as poorly as the burned C. scabra, Sommer possibly resulting from traumatizing the animals when removing them from the rock. A set of lab experiments was therefore done, where disturbance to the limpet was minimized. 8 C. scabra, maintained in the sea-table and observed over 5-11 "high tides" to forage and to home consistently during this period, were used as subjects. Controls were 30 other limpets which had been similarly observed in the sea-table. When an experimental C. scabra was foraging at least 5cm away from its home site, its rock was tilted so that the limpet was barely submerged. Then an area around the home site about 4-5cm in radius was heated intensively with a propane torch. The rock was then re-submerged, and the sea-table was allowed to drain slowly in simulation of a falling tide. 5 out of 8 limpets returned to their burned-out home sites with no apparent hesitation in comparison to the controls. 2 Of 3 non-homers returned to the area of the home site, but while traversing the heated region, encountered patches of a crumbly brown substance, possibly an encrusting alga burned by the heating process. The animals did not traverse this substance, but turned away from it, or attempted to reach the home site from another approach. This was not possible beeause these patches completely surrounded the home sites. The remaining non-homer did not even turn around to head toward home upon the onset of "low tide," as the others had done. This limpet may have been disturbed by the heating, or it may have been in the process of changing its home site. Displacement experiments. All of the previous experiments involved limpets homing on their Sommer own rocks, whether in field or in the lab. In the following experiments, limpets were taken from the field and placed on glass or rock in the sea-table, and subjected to two high tides per day for over 3 weeks. Animals which were placed on glass ranged from.4-2cm in length. Some limpets crawled off the glass at the beginning of the study. Those which remained grew their shells to conform to the flat surface. No homing was observed. At each high tide the animals would either reorient themselves slightly, or move to a new place altogether. Within 2 weeks, the larger limpets, 1.5-2.0cm in length, had grown new shell around the bottom edge, discernible as a 1-2mm wide band of lighter, thinner shell, conforming exactly to the glass. Those limpets which were placed on new rocks were 1.0-2.Ocm in length. During the first few "high tides," they wandered on the rock, not returning to any previously occupied site (i.e., no homing). After 3-4 "high tides," the limpets merely reoriented themselves by 180° on spots which, in one direction, seemed to fit their shells fairly well. They continued this behavior regularly with the changes of the tides until, in 1-2 weeks, they began homing behavior, leaving these sites at "high tide" and returning to them at the onset of "low tide." By this time their shells conformed very well to thiser new sites. Home site transplantation experiments. A final series of experiments involved transplanting an animal and its home site to new substrate. C. scabra home sites often occur on superficial crystals in the granite. A sharp tap with a chisel Sommer 10 to the crystal/granite interface is usually sufficient to dislodge the whole crystal, complete with the limpet on its home site. A number of crystal home sites were thus removed from the field and transplanted to glass and new rocks in the sea-table. They were glued to the new substrate with silicone sealant (Figure 4). Once the limpets had crawled off the crystals onto the glass substrate, they wandered with each high tide, never returning to the region of their crystal home sites. Within 5 "high tides." 6 out of 9 limpets had left the glass altogether, the remaining 3 never having left their crystals through 20 days of observation. Varied results were obtained from observations of limpets on crystals transplanted to new rocks. After 2 weeks, 4 of 12 animals had never left the crystals, 5 had left and set up new home sites on the rock, never having moyed back in the direction of their crystals, 2 were missing, and 2 limpets had left their crystals, foraged on the rock. and returned via the outgoing path to their original home sites. Homing on these transplanted sited was thus very poor. In an attempt to reduce the possible adverse effect of steep cliffs (crystal edges) on homing ability or desire to return home, similar transplant- ation was performed, but this time the crystals were embedded in pits chiselled into the new granite so that the edges were flush with the surface of the rock. Gaps were filled in with a mixture of ground granite and glue. 2 crystals were embedded in this manner. One limpet never left its crystal in 10 days of observation. The other left and foraged on the rock, homing back to its home site at the onset of "low tide," on 3 separate occasions. The rest of the time, Sommer it did not leave its crystal. It would seem that the last method of home site transplantation would be most useful in additional future studies of this sort. Discussion Based on the results of sea-table home site-burning experiments. it appears that a complex, information-bearing chemical trail, if laid down by these limpets at all, is not necessary for homing to occur. It seems that some kind of recognition of local topography could allow the limpet to return home. It is possible, however, that a combination of trail following and topography appreciation is involved in homing behavior, not necessarily at the same time, but in sequence. as the animal develops. For example, very small, newly settled C. scabra might initially lay chemical trails on the not-yet-familiar substrate, in order to return to their home sites, "learning" the topography as they become familiar with it in foraging. Once this occurred, chemical information might no longer be necessary. The admittedly casual observations on home site transplantation and limpet displacement show that limpet homing can be studied in the lab. The fact that C. scabra were not seen to home on glass could be indicative of a need for some kind of variance in the surface of the substrate to facilitate homing via "learning" of the topography; or it may simply suggest that in cases where C. scabra conform to the surface everywhere, they do not need to home to a specific site. The limpets which were displaced were, unfortunately, not rigorously observed throughout every high tide after being taken from the field. so it is not known whether they consistently followed their outgoing 12 Sommer paths back to their homes after their initial foraging run. On occasion they were seen to return home by the same path, and toward the end of the study some animals were seen to take a circular route. Further study is warranted on this topic. Perhaps, as hypothesized above for developing limpets, the displaced animals follow a chemical trail at first, until they become familiar with the surroundings. Burning experiments could be performed with these animals as soon as they begin to forage, to test this idea. Sommer Summary 1. C. scabra less than Amm long home. The rate at which they change home sites may be greater than that of adults. 2. Homing in adults persists after burning the home site and surrounds. 3. Chemical trail following may play a role in homing of juveniles, limpets which have voluntarily changed sites, and limplets removed from the field and placed on new substrates, Sommer 14 Acknowledgments I would like to thank my advisor, Dr. W. Gilly, for encouragement and advice provided throughout this study, and also for the inspirational trips to the Seaside Dump. The assistance of the many unfortunate C. scabra who were forced to give up their homes in the name of science is also gratefully acknowledged. Sommer 15 Literature cited BRANCH, G. M. 1981. The biology of limpets: physical factors, energy flow, and ecological interactions. Oceanogr. Mar. Biol. Ann. Rev. 19: 235-380 BRANT, DANIEL H. 1950. A quantitative study of the homing behavior of the limpet Acmaea scabra. Unpubl. Spec. Prob. Reprt. Dept. Zoology, Univ. Calif. Berkeley COOK, ANTHONY Homing in the Gastropoda. Unpubl. manuscript, New Univ. Ulster, coleraine, N. Ireland HEWATT, WILLIS G. 1940. Observations on the homing limpet, Acmaea scabra Gould. Amer. Midland Naturalist 24(1): 205-208 JESSEE, WILLIAM F. 1968. Studies of homing behavior in the limpet Acmaea scabra. The Veliger 11: 52-55 (supplement) O Sommer 16 CAPTIONS TO FICURES AND TABLES Homing behavior of 26 C. scabra in 3 size classes over Figure 1. 5 daytime high tides. Figure 2. a. Schematic representation of levels of homing. b. Results of foraging runs of 26 C. scabra over 5 daytime high tides. Figure 3. Sea-table arrangement for homing studies. Figure 4. Crystal home site transplantation onto new substrates. Table 1. Results of field home site burning experiment. 5OMHER P.7 day total forays homing change of site 2° homing 3° homing 19 homing N 3-4 mm 2 — 3 mm — 2 mm changed no foraging homing site observed 12 13 change 0 2° homing 5 total tota 16 % forays 84.1 5.8 7.2 1 2 2.9 S 3 homing HER 9.18 E6.3 F16.4 SEA WATER21 EXPERIHENTAL 6 C SCABRA DN GRANITE HOULDERS 7 eue A GLASS „PERFORATED TUBING :. :. Lrus 6 L SEA-TABLE S CRYSTAL HOME 4 SITE GRANITE GRANITE g en N=9 BURNED 33.3 % 44.4 % 22.2% n = 10 CONTROLS 30 % 40% 20 % POSTTON AT Znd HIGH TIDE AFTER BURNING AT HOME SITE AWAY FROM SITE NISSING FROR ROK TAGLE