trail following in the chiton acanthopleura gemmata: operational and ecological problems

Marine Biology 95, 539-545 (1987) Marine . . . . . . . . Biology

@ Springer-Verlag 1987

Trail following in the chiton Acanthopleura gemmata: operational and ecological problems

G. Chelazzi, P. Della Santina and D. Parpagnoli

Dipartimento di Biologia Animale e Genetica dell' Universitd; Via Romana 17,1-50125 Florence, Italy

Abstract The Indo-Pacific, intertidal chiton Acanthopleura gemmata (Blainville) is a central place forager which occupies defi- nite, actively dug and defended scars, and migrates during nocturnal low tides up to 3 m away to feed on algal grounds. After each feeding excursion, most chitons home precisely to their scars. Photographic tracking, using light- emitting diodes (LED) glued to the chitons, and experiments were conducted throughout 45 d (August to Sep- tember 1984) along the Nimfl Peninsula (Somalia) in or- der to elucidate the importance of trail following in the homing and feeding of this species. LED tracking of the chitons throughout each activity phase and trail interruption experiments showed that following the personal outgoing trail is a basic homing mechanism in this species. Translocation of the chitons on a conspecific trail and homing performance analysis revealed that the trail-associated information involved in the homing is polymorphic in the population, thus minimizing the probability of following a conspecific trail despite the frequent trail crossings due to high population density. The LED tracking throughout successive activity phases showed a high coincidence between the paths traced by the same chiton night after night. In the few cases when the outgoing and return paths of the first night markedly diverge, the home-feeding ground route of the successive night overlaps the return trail of the previous night. A less pronounced inter-individual trail following also occurs during foodward excursions. These findings suggest that the trails released by A. gemmata are complex, including both quasi-individual and species-specific information. Moreover, this chiton may utilize its trail following capacity not only to home, but also for the retrieval of the feeding grounds night after night.

Introduction

The Indo-Pacific, intertidal chiton Acanthopleura gemmata migrates during nocturnal low tides from an actively dug

scar (mid-eulittoral) to algal grounds (mainly low-eulittoral) up to 3 m away (Chelazzi et al., 1983a). Scars are quasi-personal: they are reinhabited after each migratory cycle and defended against possible conspecific intruders, though moderate owner substitution occurs (Chelazzi et al., 1983b). This accurate home-related behaviour reduces the risk of predation by the toad fish Arothron immaculatus which, in the study area (east-African coast), is able to dis- lodge unsheltered chitons from rocks during high tide.

Analogous with the gastropod homing behaviour (Hamilton, 1977), deposition of a mucuous trail and its subsequent retracing can be hypothesized as a homing mechanism in Acanthopleura gemmata. Nevertheless, the trail following has never been extensively investigated in chitons, even when claimed (Thorne, 1968). The ecology of A. gemmata is centered on individual homes, but the feeding paths of different chitons often cross each other due to high population density (up to 35 chitons per meter of coast), and this poses a functional problem concerning the individual specificity of the eventual homing-associated trail information.

Two other aspects ofA canthopleura gemmata behaviour deserve attention. First, the chitons generally return close to the previous night's feeding ground (Chelazzi et aL, 1983 a), which suggests the reiterative exploitation of algal patches. Second, simultaneously grazing chitons are moderately clumped (Chelazzi etal., 1983b), which suggests a multispecimen exploitation of the same algal ground. Do these phenomena rely upon personal (previous night) or interindividual feeding-related trail following? In fact, trail following in gastropods has usually been considered in the context of homing (Cook, 1969; Cook and Cook, 1975), mate searching (Hirano and Inaba, 1980) or prey location by carnivorous species (Snyder and Snyder, 1971; Cook, 1985), while its importance as a mechanism for increasing feeding efficiency in algal grazers has never been investigated.

The present observations and experiments on A canthopleura gemmata aim at elucidating: (i) the importance

540 G. Chelazzi et al.: Trail following in Acanthopleura

of trail following in homing and its degree of individual- specificity, (ii) the possible presence of long lasting self- and (iii) hetero-trailing, for feeding ground retrieval night after night.

Materials and methods

Field recording of excursions and trail following analysis

This study was conducted throughout 45 d (August to Sep- tember 1984) on a population of Acanthopleura gemmata (Blainville) on the rocky shore of the Nimfi Peninsula (So- malia), where previous investigations on the same species had been performed (Chelazzi et al., 1983 a, b). Chitons in five selected areas were equipped with small lighters (1.2 g), consisting of a light-emitting diode (LED), a bat- tery and a plastic number encased in dental acrylic (Chelazzi et al., 1983c). In each study area, lighters were stuck to the second shell plate of 10 to 15 chitons larger than 4.5 cm during diurnal low tide (rest phase), while smaller chitons were dislodged from the shore. Continuous recording of movements was obtained by an automatic camera placed on the overhang of the rocky cliff. A series of exposures (10 rain each) covered the entire dusk to dawn period (activity phase) on two consecutive nights. Four long-lasting fighters were placed as reference markers at the corners of each study area.

Each individual path was reconstructed by back-pro- jecting the slides relative to each activity phase on a screen and digitizing every relevant position (start, end and turning points in each shot), so as to obtain a sequence of coor- dinates relative to a reference x0 and yo. Each individual file was then gridded with a standard set of horizontal fines 1 cm apart. Time relative to each position was interpolated by assuming the speed to be constant throughout each 10- min path segment. The motion parameters of each path (speed and orientation in each segment, total length, total duration etc.) were then elaborated. The coincidence between different paths, or path segments, was obtained by computing the fraction (normalized to 1) by which the presumed follower path overlapped (less than 3 cm apart) the presumed leader trail. In particular, three different analy- ses were conducted:

(i) homeward auto-trailing (HAT), i.e. the coincidence of the return path of each chiton from the feeding ground, with its own outgoing path on the same night;

(ii) foodward auto-trailing (FAT), i.e. the coincidence of the outgoing trail of each chiton, with its outgoing (FATo) or return (FATr) path of the previous night;

(iii) foodward hetero-trailing (FHT), i.e. the coincidence of the outgoing path of each chiton, with outgoing trails laid earlier by conspecifics on the same night.

Overall, as well as segmental, coincidence analysis was performed, the latter in reference to ten distinct segments of the entire supposed follower-path between home and feeding ground.

Trail interruption and translocation tests

The importance of auto-trailing in homing was tested by removing a trail segment between home and feeding ground (Fig. 2a), using one of two alternative methods: by brushing an area 20-cm-wide (normally to the path) and 2-, 5-, or 10-cm-long, just behind the chiton; or by placing a strip of thin aluminium foil (20 • 2 cm) in front of a moving chiton, and removing the strip after its passage. The presence of the chitons in their homes was then controlled at the following rest phase (diurnal low tide), but some chitons were also LED monitored. The strip method is prefer- able since it does not change the micromorphology of the rock surface; however, it did cause most chitons to stop or markedly deviate from their downward route upon contact.

The individual specificity of trail associated information was tested by moving feeding chitons on the trails laid by their conspecifics 2 to 7 m apart, after turning their long axis 180~ the displacement was usually reciprocal (Fig. 4A). As a control, some chitons were dislodged from the substrate and replaced on their own trail after being turned 180 ~ . Both the control and experimental chitons were kept for about 1 min with their foot on a Teflon sheet before being replaced on the rock and gently pushed onto the substrate until attached. Damaged chitons were dis- carded. The presence of the chitons in the expected home was checked at the following rest phase.

Results

Homeward auto-trailing

Analysis of 98 complete individual paths (Table 1) con- f rmed the three-phase pattern of Acanthopleura gernrnata excursions previously inferred by discontinuous monitoring (Chelazzi etal., 1983a). A relatively fast, outward phase begins as soon as the nocturnal low tide recedes

Table 1. Acanthopleura gemmata. Average values of motion parameters during three different parts of the activity phase (98 individual paths)

t s a r c li

0- 90 1.4 (_+0.8) 215 ~ 0.728* 0.186 0.852 90-210 0.7 (_+0.3) 92 ~ 0.055 n.s. 0.451 0.237

2 t0-300 2.0 (-t-0.9) 355 ~ 0.812" 0.870 0.864

t = time (rain) after the beginning of activity s = average speed (cm min -1) and relative standard deviation a = direction of the resultant vector of movement

(0 ~ = upward) ' r = length ofthe resultant vector. *: P<0.001; n.s.: P>0.1;

Rayleigh test (cf. Batschelet, 1981) c = fraction of path (normalized to 1) coincident with the

previous path of the same chiton during the same night li = path linearity, i.e. ratio between the distance between

two positions separated by a given time and the length of the path recorded between the two points

G. Chelazzi et aL: Trail following in Acanthopleura 541

A �9

HAT '/

outwQrd / p a t ~ . . . . . .

6 0 -

40 .>, u

0

B

n =98

[ - -

I I 0-.2 .2-./.+ ./.,-.6

HAT

I I

.6-.8 .8-1

Fig. 1. Acanthopleura gemmata. Coincidence between the return and outward path of each excursion (A) considered for the as- sessment of the homeward auto trail following (HAT). Black oval: chiton (not to scale). Frequency distribution (B) of HAT (normalized to t) relative to the whole sample of complete paths obtained by LED tracking

from the rest level (first 90 min of activity, on the average). This is followed by about a 2-h grazing phase, slow and randomly oriented with respect to home, when radular scraping on the rock is audible. The third phase (the last 60 rain of activity) is the return branch of migration, slightly faster than the outward movement and characterized by a marked coincidence with the previous path. Since the transition from the outward phase to actual feeding, and from this to the return phase, is difficult to assess precisely in the individual paths, we simply considered the first and second half of the entire path as the outward and return branch, respectively (Fig. 1 A).

The overall coincidence of the return and outgoing path is close to 1 in most cases (Fig. 1 B), indicating that auto- trailing (HAT) is a basic strategy for homing. In some in- stances, however, low HAT was observed, associated with meandering and horizontal excursions that could indicate that HAT is facilitated by geotaxis. Nevertheless, these atypical movements (tortuous, horizontal and unlooped) are an aftermath of home loss following a fight with a conspecific (Chelazzi et al., 1983 b).

The trail interruption experiments (Fig. 2) show that homing ability declines as the length of the missing trail increases, but about 50% of the chitons were still able to home at the maximum length tested (10 cm). The homing ability of chitons after trail manipulation depends on their capacity to contact again the trail on the homeward side of the interruption (Fig. 3), rather than on such non-trailing mechanisms as geotaxis. It is worth noting that the searching movements performed after reaching the interruption show frequent auto-trailing. Since brushing the trail for 2 cm produced a slightly (not statistically) stronger effect than subtracting 2 cm of trail by aluminium foil, the distur- bance due to physical manipulation of the substrate, not related to orienting cues, can be considered negligible in the brushing experiments.

The homing performance of feeding chitons, when removed from the substrate, turned 180 ~ and replaced on

A �9

( 00

8O

c

E 60 o

IB n=23

NN N

2

30 28 28

2 5 (cm)

10

Fig. 2. A canthopleura gemmata. Schematic representation (not to scale) of the trail interruption experiments (A). White oval: scar; black oval: chiton; solid fine: trail; dashed area: trail interruption. Homing performance (B) of the chitons whose trail was removed by using an aluminium sheet (shaded column) or by brushing the substrate (white columns). 1: length of missing trail. Numbers above columns indicate the size of each sample

E t )

~.. down " ~ i i ~ (seaward )

brushed ~2-_--~ area 41ff...~

~.', J ";r,,"&'

Fig. 3. A canthopleura gemmata. LED recorded path of a chiton during a trail interruption test. Shaded rectangle: brushed area. Solid line: outward path; dotted line: typical homing-related auto trail following; dashed line: searching path following the en- counter of trail interruption. Note how the coincidence with the outward path appears again when the chiton recontacts it on the homeward side of the interruption

their own trail decreased from the usual value of nearly 100% (Chelazzi et al., 1983 a) to 78% (Fig. 4). This is a fairly high performance, which excludes the use of idiothetic mechanisms (see Schtne, 1984) in homing. On the con- trary, only 10% of the chitons translocated to a conspecific trail homed to the new scar. These results strongly support a certain degree of HAT individuality, but why is homing performance not reduced to zero after translocation? Chance-finding of the home seems improbable, given the distance between the release point and scar (an average of 150 cm). One explanation could be the similarity between the information associated with the trail of displaced and marker chitons. Since experiments involved pairs of ehi-

542

A

@

/ 2+7 m i

0) i-'., z'i - ~ - - - k J I

controts expe r imen to l s

10Cr-- B

80- r

O

E 60- 2 $ O- ~0- E

E o 2 0 -

O -

n=98 92

~o. exp.

Fig. 4. Acanthopleura gemmata. Schematic representation (not to scale) of the translocation experiments (A). Solid line: trail; dashed fine: translocation. Homing performance (B) to the orig- inal (controls) and to the new home (experimentals), after the treatment. Numbers above the columns indicate the sample size

30

20

r |

13- a3

~- 1(3

n=38

I I

0-.2 .2-.4 /*-.6 .6-.8 .8- i co inc idence

between success ive excurs ions

Fig. 5. A canthopleura gemmata. Frequency distribution of the coincidence (normalized to 1) between paths on two consecutive nights

G. Chelazzi et al.: Trail following in A canthopleura

tons, a concordance could be expected in their homing ability. Sample size was too small to give significant evidence, but out of nine successful returns, six were scored by three pairs.

Path constancy night after night and foodward auto-trailing

The overall coincidence between the path traced by 38 chitons on two consecutive nights was computed (Fig. 5). Though the coincidence is not as deterministic as the HAT (Fig. 1 B), what is impressive is that 23% of the paths diverge only slightly and very distally from that of the previous night. This could be due to a chance coincidence between successive paths, given their common origin and generally vertical orientation, or to a strong channeling effect caused by a marked anisotropy of the substrate. How- ever, the observed coincidence is not related to the linearity and verticality of the trails (Fig. 6), and careful in- spection of the shore revealed no important morphological anisotropy: except for the home neighbourhood, the substrate on which chitons migrate is very regular.

Is there a difference between FATo and FATr: i.e. does the foodward path of one night overlap more the outgoing or the return branch of the previous migration (Fig. 7A)? Though usually the coincidence between outgoing and return trails on the same night is high, the average FATr values are slightly larger than the corresponding FATo between the fifth and eight tenth of the home-feeding ground distance (Fig. 7B). Moreover, in the few cases where the outgoing and return branches of the first night showed a marked, early divergence, the chiton followed the return trail (Fig. 8).

Foodward hetero-trailing

1 . 0 - -

O

.8

x

"13 O1

U �9 ~ = tN r -

.2

$

I P

�9 �9 dP

�9 l

t o

�9 ~ I �9 1 1 1 1 ~ | 1 t I 0 .2 .4 .6 .8 1.0

ti. cos @ Fig. 6. Acanthopleura gemmata. Coincidence between paths recorded during two consecutive nights (ordinate), plotted in func- tion of the product of linearity of the second path by its verticality (abscissa). The linearity (li) is computed as in Table 1. Verticality has been obtained by considering the segment of the second night connecting the starting point (scar) to the mid-excursion point (feeding ground). Theta: minimum angle between this segment and the vertical

Out of 98 fully recorded paths, 62 contacted one or more trails laid by conspecifics during the same activity phase. The coincidence between the foodward path and conspecific trails (FHT) is not conspicuous, except in a few cases (Fig. 9) which could be explained by trail information similarity. In fact, some of the high FHT trails prelude home intrusion or home exchange. However, considering the 50 trails characterized by an FHT larger than 0.15, it is evident that chitons may follow more than one distinct leader trail during their outgoing migration (Fig. 10). The observed FElT could also be due to substrate anisotropy, but this explanation seems untenable as previously discussed. The relative importance of the auto- and the presumed hetero-trailing during foodward migration was analyzed from 38 paths, 29 of which showed an overall FAT larger than FHT. However, the segmental analysis shows that FHT importance increases at increasing distances from home and is larger when approaching the feeding ground (Fig. 11). From the same figure it is evident that the path fraction free from auto- or hetero-trailing is relatively small throughout the migration.

G. Chelazzi et aL: Trail following in Acanthopleura

A

.f~176176176176

f 2rid outward, / ; . ' ~ outward

i O " " k - )

1st'.. t r e t u r n " . . . ' "

1.0

.8

< . 6 LI_

>

.2

[ i i I

2nd outward path home ( tenths )

q feeding ground

543

Fig. 7. Acanthopleura gemmata. Schematic representation (not to scale) of the foodward auto trail following (FAT) (A). Average segmental values (and 95% confidence interval) of the coincidence between the outward path recorded during one night and the outward (FATe, black dots) or return (FATr, white dots) path of the previous night (B)

' - . . . . . '~176176 i

*" , : ' " v ,

down (seaward)

Fig.& Acanthopleura gemmata. An example of marked divergence between outgoing (solid line) and return (dotted) branches of the same path (A). The path of the same chiton (B) during the following night. Note the coincidence between the second path and the return branch of the former. A and B paths are represent- ed as shifted (open arrow). Black ovals: the chiton at home

50

40

>,30

g20

10

n:50

r 1 2 3 4

n.of trackers

Fig. 10. Acanthopleura gemmata. Frequency distribution of the number of different leaders followed by each chiton during its outward migration. Only the chitons with overall FHT >=0.15 have been considered. In the case of multiple coincidence with more than one leader, the coincidence was scored only once, with reference to the leader which had first traced that segment

/,0

30

~= 20

g

10

n:62

I I

0 -.2 .2_/* .4-.6 F l IT

.6-.8 .8-1

Fig. 9. Acanthopleura gemmata. Frequency distribution of the coincidence between the outward path of one chiton and the trails laid earlier by its conspecifics during the same night (FHT). Co- incidence of the same segment with more than one leader trail was scored only once

Discussion

The operat ional and ecological aspects o f our findings on Acanthopleura gemmata will be discussed with reference to gastropods, since no exper imental evidence on the trail following is available for chitons.

Operat ional aspects

The analysis of paths of undis turbed chitons, the homing performance of control (only turned) chitons, and the homing impai rment after trail in terrupt ion leave no doubt about the impor tance of following the self-trail in the homing of Acanthopleura gemmata. Other orienting mechanisms cla imed for the homing of some gastropods, such as idiothetic orientat ion (Pieron, 1909), topographic memory (Ohgushi, 1955; Thorpe, 1963; Galbra i th , 1965) or cues not associated to the substrata (Bohn, 1909), are - i f present at

FATr [

o,

return :

544

f, g

1 0 0 - B

80

60

40

2O

0 1

home

2 3 z, 5 6 7 8

2nd outward path tenths

9 10

feeding ground

G. Chelazzi et al.: Trail following in A canthopleura

Fig. ll . Acanthopleura gemmata. Schematic representation (not to scale) of the foodward auto-(FATr) and hetero-(FHT) trail following (A). White ovals: scars; black oval: trailer chiton; shaded oval: leader chiton. Seg- mental percent frequency (B) of cases in which FATr> FHT (black columns) and FHT> FATr (white columns). The cases when FATr and FHT< 0.15 are rep- resented by missing percentage to 100%

all - of secondary importance for this species. Coupling the LED monitoring to the homing performance analysis after trail interruption is particularly interesting in this respect: it suggests that the high homing performance of some gastropods after trail manipulation (Galbraith, 1965; Jessee, 1968; Cook etal., 1969) cannot prove the importance of nontrailing mechanisms in their homing.

A certain degree of individual specificity of HAT is also evident from the present data. Corresponding evidence is contradictory for gastropods: among the few species whose trail-individuality has been explicitly investigated, Patella spp. (Funke, 1968) and Onchidiumfloridanum (McFarlane, 1981) discriminated between personal and conspecific trails, while nonindividuality was found in Siphonaria alternata (Cook, 1971) and, obviously, in collective homers such as Nerita textilis (Chelazzi etal., 1983c, 1985) and Bursatella leachii (Lowe and Turner, 1976).

The displacement experiments performed on Acan- thopleura gemmata show that a quasi-individuality (low trail polymorphism) could be involved in its HAT, rather than an absolute individuality: eight different trail types in the population could be enough to produce the observed difference between control and experimental chitons. This rough estimate is open to further investigation.

The foodward auto-trailing, never explicitly analyzed in algal grazer gastropods, requires a long-term stability of trail information, given the time lag between two successive excursions in Acanthopleura gemmata (18 to 20 h). Among intertidal gastropods, survival of trail information through one or more days has been reported in Siphonaria spp. (Cook, 1969, 1971) and Nerita textilis (Chelazzi et al., 1985).

The possible discrimination between the outgoing (FATo) and return trails (FATr) of the previous night is the second important operational aspect of Acanthopleura gemmata trail following that deserves further quantitative analysis. Such a discrimination could be based either on the difference in informational content between the different path segments, such as that found in Onchidiurn ver- rucutatum (McFarlane, 1981), or on the intrinsic polariza- tion of the trail, such as that found in different gastropods (cf. Stirring and Hamilton, 1986).

Finally, does a foodward hetero-trailing exist and, if so, what is its functional basis? The apparent contrast between auto- and hetero-trailing could be resolved by admitting that the trail of Acanthopleura gemmata contains both quasi-individual and species-specific information, and that the chitons are able to follow either their own or a conspecific trail depending on their motivation. This hypothesis is

highly speculative, but modulation in following trails of a different nature has been observed in the land putmonate Euglandina rosea (Cook, 1985).

Ecological aspects

The ecological significance of the quasi-individual HAT is evident for a solitary homer such as Acanthopleura gemmata, whose adaptation to the intertidal environment ro- tates around the ownership of personal shelters (Chelazzi et al., 1983 b; Chelazzi and Parpagnoli, in press). The ownership of individual scars and related homing in intertidal gastropods has been considered as a factor increasing their resistance to various physical and biological stress factors (Cook, 1976; Branch, 1981; Creese, 1981).

More open is the problem of FAT. This capacity may permit: (a) feeding ground retrieval night after night with a consequent reduction of exploratory movements, and associated energy and time cost, or (b) the reduction of the number of trails connecting the home to the feeding grounds. The benefit related to (a) could consist in the reduction of time spent out of the home, with a consequent reduction of the risk of home intrusion by conspecifics. Al- so (b) can be interpreted as a strategy against intrusion, since the compactness of the trail web spreading from home reduces the probability that a conspecific could contact a trail and follow this to the scar.

It is obvious that following the return branch of the previous excursion (FATr) could allow a very efficient retrieval of suitable feeding grounds if the chiton could modu- late the emission of orienting cues according to the quanti- ty or quality of the most recently exploited algal ground. That FATr is not deterministic in Acanthopleura gemmata could be highly functional in permitting the discovery of

G. Chelazzi et al.: Trail following in A can thopleura 545

new algal patches. A similar hypothesis has been expressed for ant recrui tment (Deneubourg et al., 1983). The adapt ive value of a probabil is t ic foodward trail following is even more evident for the FHT: i f tuned to high levels, following conspecific outgoing trails would result in local over-ex- ploi tat ion of food resources, while its tuning on minimal levels would produce l imited inter individual recruitment.

Though many operat ional and ecological aspects of trail following in Acanthopleura gemmata remain open to further analysis, the present findings suggest that this behaviour cannot be simply considered in the context of homing; rather it is an or ienta t ion-communicat ion mechanism of mult iple significance in its adapta t ion to the in- tert idal environment.

Literature cited

Batschelet, E. B.: Circular statistics in biology, 371 pp. London: Academic Press 1981

Bohn, G.: De l'orientation chez les patelles. C. R. Acad. Sci. 148, 868-870 (1909)

Branch, G. M.: The biology of limpets: physical factors, energy flow and ecological interactions. Oceanogr. Mar. Biol. A. Rev. 19, 235-380 (1981)

Chelazzi, G., P. Della Santina and M. Vannini: Long-lasting substrate marking in the collective homing of the gastropod Nerita textilis. Biol. Bull. mar. biol. Lab., Woods Hole 168, 214-221 (1985)

Chelazzi, G., S. Focardi and J. L. Deneubourg: A comparative study on the movement patterns of two sympatric tropical chitons (Mollusca: Polyplacophora). Mar. Biol. 74, 115-125 (1983 a)

Chelazzi, G., S. Focardi, J. L. Deneubourg and R. Innocenti: Competition for the home and aggressive behaviour in the chiton A canthopleura gemmata (Mollusca: Polyplacophora). Be- hav. Ecol. Sociobiol. 14, 15-20 (1983b)

Chelazzi, G., R. Innocenti and P. Della Santina: Zonal migration and trail-following of an intertidal gastropod analyzed by LED tracking in the field. Mar. Behav. Physiol. 10, 121-136 (1983 c)

Chelazzi, G. and D. Parpagnoli: Behavioural responses to crowd- ing modification and home intrusion in Acanthopleura gemmata (Mollusca: Polyplacophora). Ethology (In press)

Cook, A.: Functional aspects of trail following by the carnivorous snail Euglandina rosea. Malacologia 26, 173-181 (1985)

Cook, A., O. S. Bamford, J. D. B. Freeman and D. J. Teideman: A study of the homing habit of the limpet. Anim. Behav. 17, 330-339 (1969)

Cook, S. B. : Experiments on homing in the limpet Siphonaria nor- malis. Anita. Behav. 17, 679-682 (1969)

Cook, S. B.: A study of the homing behaviour in the limpet Sipho- naria alternata. Biol. Bull. mar. biol. Lab., Woods Hole 141, 449-457 (t 97 I)

Cook, S. B.: The role of the home scar in pulmonate limpets. Bull. Am. Mal. Union 1976, 34-37 (1976)

Cook, S. B. and C. B. Cook: Directionality in the trail-following response of the pulmonate limpet Siphonaria alternata. Mar. Behav. Physiol. 3, 147-155 (1975)

Creese, R.: Patterns of growth, longevity and recruitment of intertidal limpets in New South Wales. J. exp. mar. Biol. Ecol. 51, 145-171 (1981)

Deneubourg, J. L., J. M. Pasteels and J. C. Verbaeghe: Probabil- istic behaviour in ants: a strategy of errors. J. theor. Biol. 105, 259-271 (1983)

Funke, W.: Heimfindevermtgen und Orstreue bei Patella L. (Gas- tropoda, Prosobranchia). Oecologia 2, 19-142 (1968)

Galbraith, R. T.: Homing behaviour in the limpets Acmaea digi- talis and Lottia gigantea. Am. Midl. Nat. 74, 245-246 (1965)

Hamilton, P. V.: The use of mucous trails in gastropod orientation studies. Malac. Rev. 10, 73-76 (1977)

Hirano, Y. and A. Inaba: Siphonaria (Pulmonate limpet) survey of Japan. t. Observations on the behaviour of Siphonariajaponica during breeding season. Publ. Seto mar. biol. Lab. 25, 323-334 (1980)

Jessee, W. F. : Studies of homing behaviour in the limpet Acmaea scabra. Veliger 11, 52-55 (1968)

Lowe, E. F. and R. L. Turner: Aggregation and trail-following in juvenile Bursatella leachiipleii. Veliger 19, 153-155 (1976)

McFarlane, I. D.: In the intertidal homing gastropod Onchidium verruculatum (Cuv.) the outward and homeward trails have a different information content. J. exp. mar. Biol. Ecol. 51, 207-218 (1981)

Ohgushi, 1L: Ethological studies on the intertidal limpets. II. Ana- lytical studies on the homing behavior of two species of limpets. Jap. J. Ecol. 5, 31-35 (1955)

Pieron, H.: Contribution ~t la biologie de la patelle et de la calyp- trte. Le sens de retour et la mtmoire topographique. Arch. Zool. exp. gen. V str. 1, 18-29 (1909)

Schtne, H.: Spatial orientation, 374 pp. Princeton: Princeton Uni- versity Press 1984

Snyder, N. F. R. and H. A. Snyder: Pheromone mediated behaviour ofFasciolaria tulipa. Anita. Behav. 19, 257-268 (1971)

Stirling, D. and P. V. Hamilton: Observations on the mechanism of detecting mucous trail polarity in the snail Littorina irrorata. Veliger 29, 31-37 (1986)

Thorne, M. J.: Homing in the chiton Acanthozostera gemmata (Blainville). Proc. R. Soc. Qd 79, 99-108 (1968)

Thorpe, W. H.: Learning and instinct in animals, 558 pp. London: Methuen 1963

Date of final manuscript acceptance: November 11, 1986. Communicated by B. Battaglia, Padova

trail following in the chiton acanthopleura gemmata: operational and ecological problems

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