Tane (1968) lh: 1+3-63 1+3

LIMPET MOVEMENTS An investigation into some aspects of movements, especially the homing behaviour.

By T. W. Beckett*

INTRODUCTION

Several overseas workers (Stephenson 1935, Patella granularis; Thorpe, 1956 Patella depressa) have shown that some species of can relocate an established home on the shore.

Two common Auckland patellid limpets, Cellana ornata (Dillwyn l8l7) and Cellana radians (Gmelin 1791) were observed to determine their movements and homing ability.

The majority of the work was conducted in the Takapuna area, with superficial observations around Auckland's east and west coasts. (Figure l).

At Takapuna C. ornata occurred from extreme high water spring (E. H. W. S. ) to the mid-tide level. (Crassostrea glomerata zone) while C. radians occurred from high water neap (H. W. N. ) to extreme low water spring (E. L. W. S. ).

Initial observations indicated that the behav• iour patterns varied with habitat. Homing behaviour was a property of C. ornata though it was not always shown by C- ornata occupying either permanently wet crevices, or the undersides of rock overhangs. To standardise conditions only specimens on seaward sloping rock faces of 30° - 70° from the horizontal were marked and observed.

Marking methods: The dry shell and the rock surface were each marked with the same number (Roman numerals) and a dot marked on the rock at the

^Department of Zoology, University of Auckland. 1*1*

Fig 1 LOCALITY

Scale of miles

0 5 10 15 20 25 •45 anterior edge of the shell. A durable marking mater• ial was difficult to find, but Gala "More Red" No. 6 nail polish was found to remain on the rocks for up to 60 days.

Observations on marked and unmarked specimens showed no apparent ill effects on limpets marked in the above procedure.

INVESTIGATION OF HOMING BEHAVIOUR a) The Presence of Homes on the Shore: A home was taken to mean the specific area to which a limpet regularly returned. To determine whether homes existed on the shore at Takapuna, nineteen specimens were marked, and their subsequent positions recorded at successive low tides. As the results were intended to encompass the average limpet population, neither the highest nor the lowest specimens were ever marked.

Six groups of limpets were marked.

Group 1. Three C. ovnata from E. H. W. S. in the Chamaesipho ornata barnacle zone. (One large, 27 - 33 m. m. long; two medium, 20 - 26 m. m. long)

Group 2. Four C. ornata from H. W. N, on bare rock sur• faces. (All medium size). Group 3. Three C. ornata from M. T. L. (Crassostrea glomerata zone). (One large, one medium and one small, 11 m. m. long). Group k. Four C. radians from H. W. N. (All medium size, 28 - 32 m. m. long). Group 5- Two C. radians from M. T. L. (Both medium size). Group 6. Three C. radians from L. W. N. (Two medium, one small, 15 m. m. long).

These six groups were observed at intermittent 1+6 low tides during the day and night for periods of nine days (Groups 1+, 5 and 6) to three months (Groups 1, 2 and 3).

The results may be summarised as follows: i) C. ornata over 12 m. m. long were each found to occupy a confined area on the rock face to which they regularly returned when the tide receded. This area is the 's home. For each individual this constitutes the home. ii) C. ornata smaller than approximately 12 m. m. long did not possess a home. iii) No specimens of C. radians possessed a home.

One day visits were made to Whatipu, Piha and to Motutapu, Motuihe and Ponui Islands, each visit coin• ciding with a low tide period.

Specimens of both species were marked at Goat Island, St. Leonard's Beach and Cheltenham, and observed over a number of visits to determine if homes existed on these shores.

These results support the observations made at Takapuna, i. e. Adult C, ornata possess a home. Adult C. radians do not.

Discussion on the structure of the home in C. ornata. Several authors (Stephenson, 1935, P- granularis, Thorpe 1956, P. depressa and Fretter and Graham 1962, P. vulgata) mention that certain limpets possess a home, and that this may be visible as a scar on the rock surface. A scar implies either a depression eroded in the rock, presumably by the shell margins and/or the foot, or a secretion exuded onto the rock surface to distinguish it from the surroundings.

No true limpet scars were seen at Takapuna, nor was any secretion or discoloration of the rock sur• faces noted where a home existed. (Sypharochiton pelliserpentis possessed a home at Takapuna which hi was in the form of a scar with a whitish secretion at its base. This type of home was observed at Canterbury by Johns (i960)).

At Takapuna in dense areas of C. columna, C. ornata homes were readily recognisable when the moved. They appeared as oval bare rock patches in the midst of the surrounding barnacles corresponding in size to the animals' shells.

C. ornata also occurs on bare areas of basalt at Takapuna. Here they still returned to a home, although the home is indistinguishable from the surrounding rock surfaces.

At St. Leonard's beach, where the rock is Waitemata sandstone, definite depressions in the rock surface were noted, and true scars were therefore present. The Parnell grit north of Cheltenham beach, and some of the softer West Coast rocks also showed some scars, but these were generally not well devel• oped.

Whether a scar is present or not is therefore entirely dependent on the type of rock on which the limpet has its home. The absence of a recognisable scar does not appear to affect the homing ability of C. ornata.

At Takapuna C. ornata had a more permanent home than did specimens of P. vulgata observed by Orton (1929). Orton noted that scars were often abandoned by the animals that formed them, and that there was usually some movement of the limpet population from one place to another, especially on smooth damp rocks.

At Takapuna eighteen C. ornata were marked at low tide on lH. 3. 67. By the 20. 7. 67, sixteen were still on their original homes - the two that had moved were both small (ll m. m. long), and both had moved up the shore. b) The Importance of the Home to C. ornata. HQ

All adult C. ornata observed in the areas studied possessed a home, indicating that homing is an inte• gral part of this limpet's behaviour.

Over a period of four months at Takapuna, sixteen C. ornata continued to return to their individual homes. If limpets are removed from the rock surface they may successfully establish a new home, implying that the behaviour patterns are flexible.

Homing ensures that the limpets remain evenly distributed over the shore, rather than densely aggregated as in the high tidal snail Nerita melanotragus.

The home, and scar if present, has been assumed to be effective in reducing water loss through desic• cation. Observations and experiments showed that C. ornata does not die if kept off its home, nor does C. ornata minimize water loss by exactly fitting into its home, as has been classically described in the European P. vulgata.

The home probably represents a position on the shore where the limpet is most secure from inter• specific competition (for space), predation and desic• cation.

c) General Movements: Little exact data could be found in the litera• ture as to the extent of limpet movements. Stephenson (1935) is reported to have found that Patella granularis travels up to five feet and that "accuracy of performance" (to return) "falls off with distance. " Fretter and Graham (1962) report that "the whole journey will cover two feet or so, sometimes following a zigzag path. "

Stephenson (1935) found that limpets frequently returned to their homes by a different path to that taken on the outward journey. Fretter and Graham (1962) noted that limpets often but not invariably returned along their outward path. h9

Presumably these movements were noted when the animals were submerged, but no mention was ever made of this vital fact.

Preliminary observations on C. ornata and C. radians at Takapuna indicated that there are a var• iety of types of movements, and that the extent of these movements was generally much less than five feet.

The different types of movements were verified by timing the animals (with a stop watch) over a five centimetre distance.

The four types of movements observed were: i) Normal submerged feeding movements. Both species show a slow (C. radians 0. 5-2. 5 cm. / min. ) (C. ornata 0. 2-1. 5 cm. /min. ) type of movement in which the head sways from side to side and the radula is presumably scouring the substrate for food. ii) Feeding on damp surfaces at night when the tide is out. Both species show a much slower speed of movement than when submerged. iii) Returning movements. Only observed in submer• ged C. ornata returning to their homes. A much faster (1. 5-3. 0 cm/min. ) and more direct movement. iv) Submerged "avoidance" movements. Only observed with two submerged C. radians. On 19. -+. 67 two C. radians were seen to be approached by two Haustrum haustorium, each of these thaid whelks pouncing on one limpet. The limpets both sped away at 8. 0-10. 0 cm/min. (A similar reaction could not be artificially produced using a thumb and "pouncing" on C. radians).

During the investigations into the presence of homes on the shore the six C. ornata in Groups 1 and 3 were observed at intermittent low tides during the day and night over a period of two months (March- 50

April 1967).

The results of these observations showed that in general C. ornata were on their homes if low tide occurred during the day, whereas they occasionally moved off their homes if low tide occurred at night.

To investigate the extent and direction of actual movements, three groups of limpets were marked on the shore. Group A: Ten C. ornata from E. H. W. S. Group B: Eight C. ornata from M. T. L. {Crassostrea glomerata level). Group C: Ten C. radians from M. T. L.

When the tide was out observations on the pres• ence of homes on the shore revealed that C. radians on and below the Corallina "turf" level did not actually remain stationary. Because observations on movements were usually done underwater, it was only possible to study upper shore animals accurately.

All members of each group were in a line down the shore, on which slope and aspect were equivalent. Each limpet was marked and its movements from the initial position recorded at thirty to sixty minute intervals.

Observations of movements in these three groups were done on a bright day (tide in) 19-3. 67, dull day (tide in) 19-1+-67, night (tide in) 9. ^. 67 and night (tide out) 2U. U. 67.

The results of these observations are shown in Table 1, where the average maximum distances travell• ed by each group away from the home site or marking position are recorded.

In addition to the preceding observations the position of five specimens was checked every fifteen to thirty minutes under all environmental conditions.

It was possible to plot on graph paper the 51 actual path followed by each limpet. A sample plot is given in Figure 2. In the Figure the home (or initial position in C. radians) of each animal is represented by an oval. Movements above the home on the shore are represented by dotted tracks above the ovals, and movements to the right, left or below are similarly shown.

Bright Day Dull Day Night Night Group 19. 3. 67 19. 4. 67 9. 4. 67 24. 4. 67 (tide In) (tide In) (tide in) (tide out)

Average max. A 16. 3 8. 0 17. 9 10. 0 distance (cm) B 16. 1 11. 3 13. S 27. 8 moved from marking post. C 40. 6 43. 4 40. 8 32. 6

TABLE 1. THE EXTENT OF LIMPET MOVEMENTS

These observations on general movements may be summar• ised as follows: i) Both species moved whenever totally submerged, this movement being invariably above the home {C. ornata) or initial position (C. radians). ii) Both species moved on moist rock surfaces at night, the direction of this movement often being below the home in C. ornata. iii) Neither species was ever observed moving on open rock surfaces during the day. iv) The speed of movements: C. radians moves at almost double the speed of C. ornata when both are feeding. v) The extent of movements: C. radians travelled further than C. ornata from the marking posi• tion. vi) The direction of movements: Both species tended to show orientated movements in a set pattern on outward and return journeys rather than random wanderings. vii) C. ornata were usually on their homes every time the tide receded, unless moist conditions 52

Fig 2 LIMPET TRACKS

C. ornata C. radians

• \ V 50, i

40 1

i T

30

i

20

Tide in / Tide out', Tide in Tide out / 10

0 CMS

10 20 30 40 50 CMS 53

occurred at night. viii) C. ornata did not necessarily follow the same paths on their journeys to and from their homes. The higher level specimens seemed less likely to return by the same path than lower level specimens. ix) C. radians returned towards their initial posi• tion, as the tide ebbed, becoming stationary when the rocks dried.

d) Discussion on the Observed Behaviour Patterns, and some of the Experimental work undertaken. The stimulus initiating submerged movements in both species was wetting by the incoming tide. C. ornata high up the shore showed a faster response to wetting, than C ornata lower down the shore. This behavioural difference could be predicted, for the 'higher level specimens have relatively less feeding time available. Movements during submersion (Tide in). The subsequent submerged movements were invari• ably above the home or the initial position, in both species. The directional movements observed may be interpreted as avoidance of desiccation, i. e. follow• ing the water up the shore, and retreating down the shore as the tide ebbs.

The extent of these submerged movements was in general much less than the three to five feet obser• ved by previous workers. The distances C. ornata moved were rarely larger than 30 c, m. s., while C. radians tended to move double this distance (Table l).

The higher level C. ornata, by moving as soon as they were submerged, and not returning to their homes till the tide receded, managed to feed for similar periods of time to C. ornata lower down the shore.

Measurements taken did not indicate that high level C. ornata moved significantly faster than did lower level specimens. Higher level C. ornata fed over new ground continuously, as they returned to their homes by a path different to that taken on the outward journey.

The termination of these submerged movements in C. ornata occurred when the tide receded past the level of the home. High level specimens were often later returning to their homes (in relation to the tide level) than those lower down the shore. C. radians retreated down the rock face as the tide ebbed, coming to rest only when the rock face dried.

As noted previously C. ornata showed a returning movement, which was initiated by the animal being exposed to the air for several seconds - often as a wave receded. The limpet invariably returned direct• ly to its home. Movements on damp rock surfaces (Tide out). Only rarely did either C. ornata or C. radians above M. T. L. {Crassostrea glomerata level) move on open rock faces in daytime during low tide. C. rad• ians occupying permanent high level rock pools also stopped moving when the tide was out during the day.

Stephenson (1935) and Yonge (l9*+9) refer to limpets moving over rock surfaces on damp days, but no such movements were ever observed at Takapuna.

To determine whether movements could be induced by pouring salt water over C. ornata, five gallons were slowly poured over five members of Group B on a bright day, dull day and at night. The remaining three members of the group were controls. Movement off the home could only be induced at night, in contrast to the results of Arnold (1957) who found that P. vulgata moved off their homes during low tide in the day if splashed with salt water.

C. ornata and C. radians were found to move over damp rock surfaces at night. 55

The initiation of these movements depended on the amount of moisture present on the rocks. If the rocks were dry no movement took place, however if rain fell on these dry rocks limpets frequently left their homes on feeding excursions.

In C. ornata the direction of movements on damp rocks at night was often below their homes. (Figure 2). The advantages of moving below their homes at night are the possibility of grazing over new ground, and the lessening of desiccation further down the shore.

As in their submerged movements high level C. ornata showed a greater tendency to return to their homes by a path different from that taken on the outward journey.

The extent of movements on damp rock surfaces at night was much less than submerged movements.

The stimulus terminating such movements was uncertain. If daybreak, (and the consequent increase in drying conditions) occurred before the next high tide, the C. ornata were all resited on their homes by sunrise. In one instance six C. ornata were observed off their homes at 03-+5, yet by Okh^ all were resited on their homes although no light inten• sity, humidity or temperature differences were detected between the two observation times.

If the incoming tide covered the C. ornata before, or just after daybreak, the limpets occasion• ally remained off their homes, and the tide covered them before excessive drying conditions prevailed. C. ornata at the highest levels on the shore often returned to their homes at daybreak, regardless of the state of the tide. e) Observed Movements in relation to Homing:

Location of the home occurred in C. ornata from distances up to 30 cms. both when submerged, and when 56 exposed to the air. C. radians always returned to• wards its initial position. Recognition of the home in C. ornata. C. ornata invariably returned to their own homes. Their orientation was to their own particular home, for they often moved over other limpet homes on their return trips. Behaviour on reaching the home. Thorpe (1956) describes a P. vulgata returning to its home from 20 cms. Thorpe states, "it appeared completely orientated throughout, showing apprecia• tion of the topography of the environment, and was not dependent on a single guiding stimulus. " Shuff• ling movements have also been observed by various authors (Yonge 19^9) and imply the limpet attempting to fit into a scar on the rock surface.

None of the 72 C. ornata observed returning to their homes ever showed such a movement. All settled down on their homes very promptly.

Orientation on the Home.

C. ornata had no constant alignment on its home, frequently being found l80° out of alignment. This lack of alignment undermines the idea that limpets always fit exactly into a scar on the shore.

In C. ornata the method of orientation did not involve a trial and error basis of fitting the shell into the surroundings. Nineteen C. ornata had the outer edge of their shells carefully chipped away with a small screwdriver, yet all continued to return to their own homes accurately.

Cases of limpets returning to the wrong homes.

Only once was a C. ornata observed returning to a neighbour's home. When the resident limpet return• ed it attempted to move the intruder by pushing it for approximately twenty minutes. (Pushing has also 57 been observed by Stephenson (1935) with P. gvanulavis\ When pushing proved unsuccessful and the rocks dried, the resident took up a position alongside the intrud• ing neighbour, corresponding to the distance between their two homes.

On being covered by the next high tide the intruder moved off on a feeding excursion, while the resident limpet returned immediately to its own home and did not feed over this period. As the tide receded the intruder returned to its correct home without going near its neighbour.

Similar reactions were artificially produced by placing "foreign" C. ornata on "resident" limpets' homes. Altering the Shape of the Home • Homes in the C columna zone were easily en• larged using a wire brush. This action did not pre• vent the limpet recognising the position of the home.

The removal of the home, using a cold chisel while the animal was off on a feeding excursion, cul• minated in the animal returning to the general area where its home was, and searching for several minutes before settling down in the near vicinity. f) The Accomplishment of Homing in C. ornata:

A brief review of the distance receptors available to an archeogastropod limpet such as Cell- ana is necessary to determine how homing could be accomplished.

Fretter and Graham (1962) consider that in Patella the body is wholly receptive to overall chemical stimulation and contact, with the eyes, osphradia, tentacles and statocysts being the most important special receptors.

Eyes: Situated at the base of the cephalic tentacles, these are of the simplest nature known in 58 gastropods, comprising an open vesicle with neither lens nor cornea. Such simple organs could he used for the detection of light, and as a guide to its direction.

Tentacles: Both cephalic and epipodial tentac• les, are almost certainly of importance in a tactile sense, being in constant motion while the animal is moving. They are also possibly olfactory receptors. The presence of a true osphradium in Patella is debated (Spengel l88l, Bernard 1890), but may be regarded as well established (Fretter and Graham, 1962).

A large number of factors influencing limpet (and other gastropod) homing can be suggested. These may be broadly subdivided: i) Stimuli which could affect homing. ii) Methods of navigation. i) Stimuli which could affect homing: Stimuli such as gravity, barometric pressure, temperature, salinity, water pressure, vibration caused by water movement and biological clocks were rejected as having no direct effect on homing in C. ornata.

Humidity in the present study was measured with a hygrometer placed on the rock surface. Although this gives a good indication, it does not accurately measure the water present on the rock. The values obtained fluctuated considerably from place to place and day to day.

The moisture of the rock surface appeared to determine whether movements occurred at night with the tide out.

ii) Methods of Navigation:

Light: Newell (1953) has shown that in Littorina littorea the eyes serve as a light compass, and the animal orientates to the light direction. 59

C. ornata homed in the day or night, and this homing ability was not altered over the night of the 2U/25. -4. 67 when a total lunar eclipse occurred at 0200.

Chemoreception: Morgan (189-+), Pieron (1909) and Hewatt (19-+0), have suggested that limpets retrace their outward tracks when returning to their homes. Davis (l895) considered that the sense data used were probably olfactory, and were appreciated by the marginal pallial tentacles.

C. ornata usually returned to its home by a different path from that taken on the outward journey, so it appears that homing was not achieved by retrac• ing a trail, as by response to chemical substances previously laid down.

On two occasions the rock surface between a C. ornata and its home was vigorously scrubbed with a wire brush. The animals invariably continued to home accurately.

The possibility that the home was liberating some chemical substance to which each animal homed was also investigated. The homes of seven C. ornata were scrubbed, using detergent and a wire brush, while the resident limpets were on feeding excursions. In all cases the limpets' homing ability was unaffected.

The Presence of Adjacent animals, and zones of feeding: C. ornata at Takapuna frequently exist in groups of three to six, and all the individuals make far-ranging excursions over the others' homes when feeding. Experiments were conducted involving the removal of all but one animal from four such groups. Five days later the four remaining limpets were still homing accurately.

This would dispose of the possibility considered that each C. ornata might be able to appreciate the density of the food source surrounding its home, 6o grazing away from its home till it reached areas where the food became scarcer (another limpet's territory). On encountering less food it would return to its own area.

Reorientating the home •

Hewatt (19**0) found that in the laboratory limpets could home to a scar reorientated in position.

Experiments at Takapuna on reorientating the homes of C. ornata while the animals were absent were inconclusive. All animals managed to return if the home was moved through 180° in the same position, but if it was elevated, or moved away from its ori• ginal position many animals failed to find it.

On the 19'h. 6l three C. ornata were moved (on their home) on a piece of basalt to a position 10 metres away at a similar level on the shore. On being covered by the tide one moved off the rock on to "new" ground, and never returned, eventually establishing a home 27 cms. away on an adjacent rock face. The other two stayed on their homes for the first tide. On the next tide both these limpets restricted any movements to the piece of basalt their homes were on; but by 25. 1+-67 both were ranging over the "new" territory and returning to their homes.

Removal experiments-

Several workers, Morgan (I89M, Pieron (1898) and Stephenson (1935) have conducted removal experi• ments, moving the limpets from the rock surface to a different position, and determining the number of limpets which returned to their homes.

Twenty submerged C. ornata were quickly removed from the rock surfaces when off their homes, and replaced on the same rock not more than 20 cms. above their homes. The animals tended to move in the dir• ection they were facing when they reattached to the rock. It was observed that many C. ornata did not 6i

readhere to the submerged rock surface after removal, and these limpets were carried out to sea by a reced• ing wave. Observation of these animals indicated that they did not reattach to the substrate, and they pre• sumably died.

It is probably best to consider removal as being a highly unnatural phenomenon disruptive to limpet orientation, and almost certainly culminating in the death of the animal in its natural environment.

DESICCATION EXPERIMENTS

Two desiccation experiments were conducted using C. ornata and C. radians to determine if there was any physiological difference between or within each species.

a) Different sized specimens collected from the same level and placed upside down in dry air showed that smaller specimens of both species lost weight more rapidly than large specimens. A number of small C. radians lost approximately 50% of their total weight over a twenty-two hour period. All recovered on being placed in salt water.

The results confirm observations on the shore - that no small limpets ever occur on open dry rock faces, though they feed over these areas at high tide. As the tide ebbs the smaller specimens invariably retire to a crevice. No C. ornata under 11 m. m. long were ever seen to possess a home.

b) Twenty similar sized (22-26 m. m. long) limpets of both species were collected from four levels on the shore. All were exposed to desiccation in the air on glass for twenty-four hours, with hourly weighings over the first ten hours.

There were no significant differences in percen• tage weight lost within or between species from diff• erent levels on the shore. SUMMARY

(i) Some individuals of C. ornata possess a home, to which they regularly return. (ii) C. radians was never observed to possess a heme. (iii) The results obtained suggested that C. ornata did not use light, chemoreception or topograph• ical memory as primary homing methods. (iv) No physiological differences between or within C. ornata and C. radians over their tidal range were detected from a desiccation experi• ment in the laboratory.

The numerical results are available from a Zoology IIIB project "Limpet Movements" in the Biolo• gical Sciences Library, University of Auckland.

ACKNOWLEDGMENTS

Thanks are due to Dr. P. R. Bergquist for super• vising the study; and to Professor J. E. Morton for critically reading the script.

REFERENCES

Arnold, D. C. 1957. The Response of the Limpet Pat• ella vulgata to waters of different salinities. J. mar. Biol. Ass. U. K. Z6: 121-129- Bernard 1890 from Fretter and Graham (1962) British Prosobranch Molluscs. Ray Society, London. Fraenkel, G. S. and Gunn, D. L. 19*+0 Orientation of Animals. Dover Press. London.

Fretter, Vera and Graham, A. 1962 British Prosobranch Molluscs. Ray Society, London.

Hewatt, W. G. 19^0 Observations on the homing Limpet Acmaea scabra. Am. Mid. Nat. 24: 205-8. •Johns, P. M. i960 Chiton pelliserpentis. M. Sc. thesis. University of Canterbury. 63

Morgan, C. L. 189-+ Introduction to comparative Psy• chology. London. Morton, J. E. 1958 Molluscs Hutchinson University Lib. London. Newell, G. E. 1958 Papers on littorina. J. mar. Biol. Assos. U. K. 37, 229-239. Orton, J. H. 1929 Observations on Patella vulgata. PT. III Habitat and Habits. J. mar. Biol. Ass. U. K. 14, 277-289. Pieron, H. 1909 from Thorpe 1956. Learning and instinct in animals. Methuen. London. Southward, J. A. 1965 Life on the Sea Shore. Heine- mann. Educational Books Ltd. London. Stephenson, T. A. 1935 from thorpe 1956. Learning and instinct in animals. Methuen. London. Spengel, l88l from Fretter and Graham 1962. British Prosobranch Molluscs. Roy. Soc. London. Thorpe, W. H. 1956. Learning and instinct in animals. Methuen. London. Wells, M. H. 1956 Learning in Marine Invertebrates. Advances in Marine Biology. Vol. 3. Yonge, CM. 19-+9 The Sea Shore Collins1 New Natur• alist. London.