[Ànalysis of Movement Patterns and Orientation lechanisms in Intertidal and [Gastropods .

Guido Chelazzi, Stefano Focardi (*) and Jean-Louis Deneubourg (**) University of Florence, Italy (*) I.N.B.S., Ozzano, Italy (**) Free University of Brussels, Belgium

fWTRODUCTION

Despite their différent organization and biology, chitons (, EPolyplacophora) and gastropods (Mollusca, ) share a large number [of adaptations Lo intertidal life, including morpho-functional and ibehavioural traits. Communication, clustering, aggresslveness and even [sltiple parental cnres have been reported in both classes but, as in other [inlmals, the basis of their behavioural adaptation to the intertidal fenvlronment is a proper organization of activity in space and time.

The quantity of reports on thèse topics is impressive, but the number [of satisfactory ethological analyses is low. The présent contribution is not [a comprehensive review of chitons' and gastropods' behavioural ecology (partial reviews may He found in Boyle, 1977 ; Newell, 1979; Underwood, 1979; Branch, 1981; Hawkins and Hartnoll, 1983), but rather is an attempt to clear liipsome conceptual and methodological misunderstandings and shortcomings, ind to identify the problems in a field that only recently has been opened toquantitative and expérimental Investigation.

[ACTIVITY ORGANIZATION IN TIME AND SPACE

In approaching the study of activity patterns of intertidal chitons and I gastropods we must clearly distinguish between occasional, continuous and rhythmic phenomena. Occasional activity includes movements in response to [ such unpredictable ecological variations as those produced by storms or the sudden appearance of predators and competitors. It also includes the Icapacity shown by somc neritid (Chelazzi and Vannini, 1976, 1980), trochid I (Byers and MitCon, 1981; Doering and Phillips, 1983) and littorinid (Gendron, 1977; Hamilton, 1978a) gastropods to regain their optimal zonation I upon expérimental displacement. A second class of occasional behaviours is I given by the avoidance responses elicited in gastropods by contact with, or the approach by potencial predators such as sea-stars (Burke, 1964; Feder, 1967; Branch, 1979) or other gastropods (Hoffmann et al., 1978).

173 -'1 Onthogenetic shifting of the population members along the shore produces an évident size-gradient in many gastropods (Branch, 1975b; Underwood, 1979) but the relative importance of individual behaviour (continuous, progressive migration along the sea-land axis) and sélective mortality in producing it has not been fully clarified.

Rhythmic activity includes movements related to seasonal, synodic, tidal and diel fluctuations in the shore ecology, Seasonal and synodic movements usually consist in zonal migrations up and down the shore in order to minimize the exposure to stress factors and to optimize the access to resources. Seasonal migrations related to reproduction have been reported in many intertidal gastropods includlng limpets (Branch, 1975b), throchids (Underwood, 1973) and littorinids (Smith and Newell, 1955; Branch and Branch, 1981). Limpets avoid dehydration and overheating by moving along the sea-land axis in synchrony with seasonal or spring-neap cycles (Breen, 1972; Branch, 1975b, 1981), but the ethologlcal determinism of thèse long-term rhythmic migrations has yet to be deeply investigated (Hamilton, 1985).

The short-term activity of intertidal chitons and gastropods is organized into temporal units determined by tidal and diel variations of physical and biological factors on the shore. In gênerai, intertidal animais] raay adopt one of two alternative stratégies (Chelazzi and Vannini, 1985). The "isophasic" pattern, typical of such mobile groups as arthropods and vertebrates, consists in rhythmic zonal migrations synchronous and concordant with the tides. Thèse animais perform a dynamic colonizacion of the intertidal environment, following oscillations in the médium (air or water) to which they are primarily adapted. Some sandy beach whelks, such as | Bullia digitalis and _B. rhodostoma (McLachlan et al., 1979; Brown, 1982) adopt this isophasic pattern, performing wide "Donax like" migrations. On a shorter scale the isophasic pattern is also shown by some littorinids as thej marsh periwinkle Littorina Irrorata (Hamilton, 1977) and the cerithid Cerithidaea decollata climbing on mangrove trunks (Cockroft and Forbes, 1981).

On the contrary, most typical rocky shore chitons and gastropods, due to the high energy cost of their locomotion (Denny, 1980; Horn, 1986) and low speed, adopt an "isospatial" strategy, remaining within a more or less narrow belt along the sea-land axis, with alternating exposure to air and water. The activity of thèse animais is limited to the time when the condition of their zone is suitable for moving and feeding. Timing of unit phase of activity (u.p.a.) is limited by the morpho-functional organization of the différent , but the very local structure of the environment, including complex relationships with other species is déterminant as well (Thain, 1971; Spight, 1982). For this reason a generalization is not possible (Hawkins and Hartnoll, 1983). Among the few chitons studied, the timing of u.p.a. includes tidal and diel components. While the latter seea to predominate in Nuttalina californica (Nishi, 1975), a tidal rhythra has been reported in Mopalla llgnosa (Fulton, 1975). In gastropods the relative importance of diel and tidal components may dépend on their zonation on the shore (Zann, 1973a).

Nevertheless, most intertidal chitons and gastropods show combined diel-tidal rhythms of high complexity (Zann, 1973b). As diel and tidal cvcles have not the same period, a short-term survey is generally not sufficient to understand the interlocking of the two components in u.p.a. timing (Cook and Cook, 1978) and a satisfactory analysis may require a complète synodic period (about 29 days). Moreover, a marked variation in u.p.a. timing can occur in taxonomically related species, and between différent populations of the same species, as in Patella vulgata (Hawkins j and Hartnoll, 1983). Careful investigation of u.p.a. timing, including th»|

1 74 Wferent sources ol' v,i r inbi 1 i ty is very important, because the t ime Sictually devotcd to feeding is a critical parameter in the energy balance of ^«tertidal gastropods and chitons; in addition, u.p.a. définition is lecessary for proper si'heduling of position sampling for movement analysis.

On the basis of the existing heterogeneous évidence, the feeding atcursions performed bv rocky shore chitons and gastropods during each i.p.a. are generally r.lassified into three distinct models of increasing •plexity: ranging pnttern, zonal shuttling and central place foraging.

Ranging pattern. In the first model, sometimes reported as "random Ipittern", feeding excursions are not orientated toward constant directions Ind the animais do not return to their previous shelter or to the sarae shore llevel. This model has been reported by Underwood ( 1977) in some australian l|JStropods and seems to be présent in some littorinids as well (McQuaid, 1981; ifetraitis, 1982). An example of ranging pattern in chitons has been found lïlth the caribbean Acanthopleura granulata (pers. observation) showing lUghly meanderlng feeding paths and no long-term preferential rest sites, flore generally, this model may be common in species living on non-tidal [ihores, or when adaptation to the littoral environment is based on the ftenporal more than spatial organization of activity, linked to a solid fiorpho-functional specializatlon to stable microhabitats. Nevertheless, [ranging does not mean random: the random walk of thèse animais must be [blased at least by kinetic responses, allowing the long-term stability of ftheir zonal distribution.

Zonal shuttling. The second model, sometimes quoted as "tidal rilgration", has been dcscribed in such gastropods as neritids (Vannini & Chelazzi, 1978; Chelazzi, 1982; Chelazzi et al., 1983c), trochids (Wara & fïright, 196A; Micallef, 1969; Thain, 1971), planaxids (Magnus and Haacker, 1968), and some 1 impets such as Acmaea llmatula (Eaton, 1968), A. pelta (Craig, 1968), .j,. scabra (Rogers, 1968) which loop along the sea-land axis it each u.p.a. Tliat this shuttling is not a true tidal migration typical of Isophasic animais is évident from the fact that - despite their upshore cUmbing for resting - many intertidal gastropods such as textilis ire splashed by waves during high tide. In some species shuttling is psradoxically inverted with respect to the sea level oscillations, with upward movements during low tide, and downward migration prior to high tide, «s in polita (Chelazzi, 1982). Zonal shuttling is due to the séparation of feeding and resting zones along the sea-land axis, not simply dépendent npon obvious physical factors: prédation and compétition more often than a simple escape from air or water are probably involved in the évolution of this pattern in such shuttlers as many trochid and neritid gastropods (Thain, 1971) and Acanthopleura spp. chitons (Chelazzi et al., 1983a).

Central place foraging. Resting in a definite shelter more or less constant in time and homing to it after each feeding excursion has long slnce been described in limpets (Davis, 1895) and chitons (Crozier, 1921). linderwood ( 1979) and Branch (1981) reviewed the occurrence, ecological significance and some operational aspects relative to the so-called "homing behaviour" of limpets, but generalization on the three aspects is again difficult because detailed analysis of movements performed by homer species during each u.p.a., and the modification of individual strategy in time, is often lacking. The sampling of only rest positions is fréquent in thèse studies, since most limpets rest during diurnal low tides, when the shore is accessible for study, while the feeding phase often occurs while the animais are splashed by waves. Thèse sampling limitations produce a fuzzy picture of the spatial behaviour.

Most contributions are concerned with the accuracy of homing performance, scaling the observed behaviour from the "statistical homing" of

175 e.g. Acmaea dlgltalis (Frank, 1964) to the deterministle homing of such ANALYSIS species as Patella depressa (Cook et al., 1969), P. vulgata (Bree, 1959), P^. longicosta (Branch, 1971), Collisella scabra (Hewatt, 1940) and Notoacmea petterdi (Creese, 1980). Similar scaling bas been observed between congeneric chitons as well (Focardi and Chelazzi, in prep.). But the following aspects of central place foraging are also important: use of natural shelters or active digging of scars, such as in many limpets (Branch, 1981) and the Acanthopleura gemmata (Chelazzi et al., 1983a); scar-shell complementarity, as in most limpets, or non-individual scar morphology permitting Its use by différent conspeclfles, as in chitons; scar défense from intruders as in Acanthopleura gemmata (Chelazzi et al., 1983b; Chelazzi and Parpagnoll, 1987) or simply abandoned upon intrusion as in A. brevispinosa (personal observation).

Moreover, the knowledge of actual movement pattern between two rest events is critlcal, giving a great deal of information on the spatial relationships between rest site and feeding grounds. It is évident that feeding loops are variously orientated in the différent species and in the différent populations of the same species: radially distributed around the shelter, as in Patella vulgata (Hartnoll and Wright, 1977), or biased along the sea-land axis as in Acanthopleura gemmata (Chelazzi et ai., 1983a). Moreover, some species are territorial, defending their feeding ground (Stimson, 1970; Branch, 1981), while in others the feeding grounds are not Personal. The long-term strategy of homers is very interesting as well, as stressed by Cook and Cook (1981): do the animais intensively exploit a good algal patch or is their feeding conservative, shifting to différent places on différent excursions? Réitération in time of individual route recording may reveal interesting aspects of homing pattern, but so far this kind of analysis has been limlted to two chitons (Chelazzi et al., 1983a) and two slphonarid limpets (Cook and Cook, 1981). A more detailed analysis of movements may help to interpret the shifting from solitary homing to collective refuging, as observed in many intertidal gastropods and some chitons. This transition often seems intraspecific and dynamic; the mechanism for shifting from solitary to collective resting must be searched for in the amplification of minimal variations in individual behaviour, depending on variations in shore morphology and tidal régime (Chelazzi et al., 1985; Focardi et al., 1985a, 1985b).

An ethological approach to ail the above aspects is more necessary than a blind classification of homing performance to understand the homing phenomenon in terms of "central place foraging" theory (Orians and Pearson, 1979). One of the methods which may open some ethological black boxes of the homing phenomenon in chitons and gastropods is LED tracking (or motographic method) (Chelazzi et al., 1983c; 1987). This simple technique permlts the intégral recording of the spatial strategy of the single animais, provided that the diel component of their u.p.a. is nocturnal. If exported to other species LED tracking may overcome many of the methodological shortcomings indicated by Hamilton (1978b): "absence of data on individuals, lack of multiple position records for individuals, Impreciseness of direction and distance measurements, small sample size, short-term observations, and lack of statistical analysis". The last point is a very critlcal one, as recently stressed by Underwood and Chapman (1985).

But establishing three very distinct models (ranging, zonal and homing) may be misleading. In fact, the zonal pattern is frequently linked to solitary or collective homing (Magnus and Haacker, 1968; Vannini and Chelazzi, 1978) and, conversely, excursions of typical homers are sometime zonally polarized (Chelazzi et al., 1983c), while deterministic homing can alternate with dispersive (ranging) excursions such as observed in the chiton Acanthopleura granulata (personal observation).

1 76 YSIS OF ORIENTATION MECHANISMS

A fréquent outcomc of the study on movement patterns is the analysis of «rlving orientation mechanisms. Intertidal molluscs have not escaped this nd and some work has been done on mechanisms controlling the behaviours cribed above. Nevertheless, the quality of information available on tons and gastropods is disappointing in comparison to that on other ps such as crustaceans (Herrnklnd, 1983; Pardi and Ercolini, 1986), with resuit that chitons and f;astropods make only a timid appearance in ent important rcviews on orientation (Jander, 1975; Schone, 1984).

Dlrectional orientation• Under the distinct sea-land asymmetry faced by rocky shore clii.tons and «astropods, there is probably no pressure to Ive such complex dlrectional mechanisms as the astronomical and magnetic entation used by some sandy beach arthropods. Some spéculations about the stence of "solar orientation" in gastropods (Warburton, 1973) must be scarded on the basis of experiments conducted on neritids (Chelazzi and nini, 1976, 1980) and littorinids (Hamilton, 1978a). Also évidence for use of nagnetic field by gastropods (Brown, 1963) and chitons (Ratner, 76) is very slim. On the contrary, the importance of gravity, light and 1 movement in the dlrectional orientation of thèse groups is évident ell, 1979; Creutzberg, 1975; Gendron, 1977) but will not be reviewed re.

The real problem with thèse intertidal animais lies elsewhere: besides «nting eues, their dlrectional orientation requires a correct modulation -'^••ement polarity to be ccologically adaptive. There is early and récent -ce that zonal movemenrs of molluscs are not based on simple responses 2 single eue, but dépend on complex régulation of taxes by arrays of leasing stimuli (Chelazzi and Focardi, 1982; Underwood and Chapman, 1985). e contributions, raost on littorinids, demonstrate the dependence of to- and geotaxis polarity on such external factors as hydration anloch and Hayes, 1926; Kristensen, 1965) and température (Bingham, 72; Janssen, 1960; Bock and Johnson, 1967), but other physical and lological releasers raay be involved as well. Endogenous reversing of taxis Issuggested by observation of movements in such shuttlers as Nerlta polita "Chelazzi, 1982), but while the internai rhythm of gênerai motor activity sbeen demonstrated in some gastropods (Zann, 1983b; Rohde and Sandland, 176) the endogenous control of cycllc reversing in photo- and geotaxis larity is a fiold npen to future research.

Homing mechanisms• Three sets of orientlng eues have been suggested to k Involved in the homing of chitons and gastropods: internai to the animal (Pieron, 1909), pertaining to the macrosystem (Bohn, 1909) or related to the llcrosystem onto which the animal moves. Once discarded the importance of JJlothetlc mechanisms, and of path-integration based on gravity or sun (Cook, 1969), two possible mechanisms of pilotlng by local information have miained: mneraotaxis, i.e. memorization of micro-landmarks intrinslc to the nbstrate, and trail following. The mnemotaxis hypothesis (Ohgushl, 1955; Piorpe, 1963; Galbraith, 1965; Jessee, 1968) rises where trail followlng tills and no direct proof of Its valldity has been obtained. On the tontrary, évidence in support of trail followlng in solitary (Funke, 1968; Cook et al., 1969; Chelazzi et al., 1987) and collective homers (Lowe and hrner, 1976; Gilly and Swenson, 1978; Trott and Dimock, 1978; Raftery, 1983; Chelazzi et al., 1985) is solid, but incomplète accordlng to some Mthors.

The followlng observations are usually reported as disproving the mlque importance of trail followlng in the homing of intertidal chitons and pstropods: 1) in some homer specles the return and outgolng paths durlng Mch feeding loop do not ovcrlap (Beckett, 1968; Cook et al., 1969; Thomas,

177 1973); il) some chitons and limpets passively displaced from their scars i possibll nonetheless able to home (Thorne, 1968; Cook, 1969); iii) différent methw and spec of trail interruption - including rock chiselllng, brushing, or washing vrfj of own ti various chemicals - fall sometimes to extinguish the horaing performance trail, SI (Galbraith, 1965; Jessee, 1968; Cook et al., 1969). But the flrst two journey. counter-proofs fail by admitting that the trail associated information Is long lasting and that animais are able to detect a previous, old trail. Trai fact, there is increasing évidence that this is true in siphonarid limpetlj concernlr (Cook, 1969; 1971) and in neritids (Chelazzi et al., 1985). Concerning thij Hamilton, third point, it is interesting what has been observed in the opisthobranckj shuttllnf Onchidium verruculatum (McFarlane, 1980, 1981) and in tht- chiton may be di Acanthopleura gemmata (Chelazzi et al., 1987): upon reaching the Neverchel expérimental trail interruption thèse animais perform exjjlorative raovenienM trail foJ which allow them to re-contact the outward trail and home safely. Cook, 197 f oHowinf Trail associated orienting eues. Although thèse considérations stronj for this support the importance of trail following in the homing of chitons and :the trail gastropods, the nature of orienting eues contained in their trails and thi |; physical actual orientation mechanism are still unknown. Cook (1971) quotes three- Pthe trail posslbilities: radular scrapings on the algal cover; textural dis- illsted th continuities provided by the mucus; attached or diffusible chemicals. Maifl -chemical authors favour the chemical hypothesis and Funke ( 1968) admits also that I ' reflectlr complex chemical "footprint" is left by Patella vulgata in the scar, in 1 Bechanisir order to correctly orientate while resting. Contact chemoreception using^ lof trail pedal receptors has been claimed for Ilyanassa obsoleta (Trott and Dimo |fIndlngs 1978), while the cephalic tentacles would be sensitive to trail associatlj Jthose of chemicals in littorinids (Peters, 1964; Hall, 1973). Raftery (1983) J«acro-gra maintains that chemical information could be important in Littorina RPlnally, planaxis, but in his opinion physical properties cannoc be ruled out. Ont RSjjihonari other hand, Bretz and Dimock (1983), on the basis of one of the most complète surveys of trail eues in gastropods, conclude chat 1 lyanassa I Trai obsoleta uses mechanical information (textural properties of the mucus) |£ollowinp not such chemicals as profeins. But in a similar analysis, performed on I llffcrent freshwater snail Biomphalarla glabrata, Bousfield et al., (1981) reachedj Inyder, 1 opposite conclusion that "chemical, as opposed to physical factors, playj |ln the ce dominant rôle in trail following behaviour". The physical hypothesis is ROnlng me indirectly supported by the observation of micro- and macro-patterning oP lew. Tha the mucus trail of gastropods (Cook, 1971; Bretz and Diraock, 1983; Stirlll] ind retur and Hamilton, 1986). But chemical content of the trail is eve:i more complj |y«rrucula including such différent classes of light and heavy molécules as free fentimna t a. aminoacids, lipids, carbohydrates, free proteins and glycoproteins (WilK putward a 1968; Hunt, 1970; Grenon and Walker, 1980, Bretz and Dimock, 1983). Futil bbservati research must proceed both ways but chemical hypothesis seems more KIM usual attractive upon récognition that the trail associated information is follow complex, including individual eues and polarity. |1uit wher s, »»^lap. Trail indivlduality. Collective refuger species are expected to xtU [tfferent and follow non-individual trails for homing. In fact this is the case fo( the In Ilyanassa obsoleta (Trott and Dimock, 1978) and Nerita textilis (Chelazi al., 1985). On the contrary, some mechanlsms for own-trail récognition r' What exlst in solitary homers, given the possible interindividual crossing ofj this f différent feeding paths under natural conditions. Some widely quoced explo experiments of Funke (1968) show discrimination between personal and as de conspecific trails in Patella vulgata and the same is crue for OnchidlU !.. 1987 verruculatum (McFarlane, 1980>'. Gross-trailing tests in Acanthopleura pillty c> gemmata (Chelazzi et al., 1987) showed that this solitary-homer chltonl illty o quasi-personal trail: a low trail polymorphysm in the population testedj tdcnce would allow the réduction of inter-individual mistakes in following thr Jlng g ,1 ' • 1 outward trail for homing. Nevertheless, other solitary-homers such as !• avol Patella vulgata (Cook et al., 1969) and Siphonaria alternaca (Cook, 197| jnlca transplanted onto conspecific trails do follow them u|) to the scar. IheJ llaclo

1 78 possibility remains that in thèse species trail contains both individual- and species-speclfic information, but in some cases the normal récognition of own trail during the homing could be based on mechanisms external to the trail, such as memorization of the direction taken during the outward journey.

Trail polarity. That trail following is not performed at random concerning polarity has been documented in many gastropods (Stirling and Harailton, 1986). When central place foraglng is combined with zonal shuttling as in K'erita textilis (Chelazzi et al., 1985), correct following aay be due to directional mechanisms based on eues external to the trail. Nevertheless, some experiments have ruled out the possibility that polarized trail following is based on such external eues as light or gravity (Cook and Cook, 1975), but the intrinsic mechanisms involved in polarized trail following have not been discovered . Cook (1971) spéculâtes four hypothèses for this capaclty in siphonarid limpets; i) chemical macro-gradient along the trail; ii) polarized séquence of différent Chemicals; iii) polarized physical structure of the trail; iv) differential friction upon retracing the trail in the two opposite directions. Stirling and Harailton (1986) listed three more: v) chemical micro-gradient; vi) bilatéral asymmetry in chemical or physical properties of the trail; vii) differential light reflectlon in the two opposite directions of the trail. By excluding other mechanisms, the last Authors conclude that a micro-structural polarization of trail is possibly detected by Littorlna irrorata. This agrées with the findings of Bretz and Diraock (1983) on Ilyanassa obsoleta, but contrasts those of Gilly and Swenson (1978) who claimed the importance of a chemical macro-gradient as polarity mechanism in Littorina sitkana and I,. 11 ttorea • Flnally, Cook and Cook (1975) obtained the Interesting évidence that in Slphonaria alternata trail polarity is lost after retracing.

Trail complexity and multiple use of trail following. That trail following may be used by intertidal gastropods in functional contexts différent fron homing, such as prey location'(Gonor, 1965; Snyder and Snyder, 1971) and mate searching (Hirano and Inaba, 1980) is well known, but In the context of central place foraging it has been usually regarded as a homing mechanism. Récent findings demonstrate that this is an oversimplified View. That homer gastropods and chitons may discrimlnate between outgoing and return trail has been argued by McFarlane (1981) for Onchidium verruculatum, and by Chelazzi et al., (1987) for the chlton Acanthopleura gemma ta. In 0, verruculatum displacement tests lead to the conclusion that outward and return tralls have différent Information content. Field observations using LED tracking showed that A. gemma ta, besides performing the usual homlng-related following of own trail, may reach the feedlng place by following Its own trail released on the previous night. What is worty is that where the outward and return tralls of the previous night do not overlap, the animal counter-f ollows the return one. This may be based on a différent Information content of the two branches as in 0. verruculatum, or on the intrinsic polarization of the trail.

Whatever the discrimination mechanisms are, the ecological Importance of this foodward auto-traillng is évident, allowing the animal to optlmize the exploitation of algal grounds. In fact the foodward trail following is not as deterministic as the homeward one. We have hypotheslzed (Chelazzi et al., 1987) that the amount of foodward trail following may dépend on the quality of return trail, which in turn may dépend upon the quantlty or quality of Ingested food. In the same species there is also prellminary évidence for inter-individual trail following in the retrieval of the feeding grounds (Chelazzi et al., 1987), which is tuned at minimal levels thus avoiding local overexploitation of algal patches. In this case communication via trail following may represent a mechanism of ecological régulation for the whole population.

179 snail Te Thèse aspects of chitons' behavlour deserve further work and the study on thèse particular topics must be extended to intertidal gastropods as Chelazzi, G., well. Nonetheless, they suggest that the trail is a complex eternal memory of on dlffe multiple ecological signifIcance, which may regulate the différent aspects 467. of central place foraging in intertidal molluscs. Besides ants, where trail Chelazzi, G., following play a major rôle in controlling the ecological relationships of in the cl chc population, intertidal chitons and gastropods may represent a second problems study case for this important class of problems in behavioural ecology. Chelazzi, G., substrat! textills. REFERENCES Chelazzi, G., interact : Nerita u Beckett, T. W., 1968, Limpet movements. An investigation into some Chelazzi, G., aspects of limpet movements, expecially the homing behaviour, Tane, 14; term zon; 43-63. (Molluscc- Bingham, F. 0., 1972, The influence of environmental stimuli on the Chelazzi, G., direction of movement of supralittoral gastropod Littorina irrorata, on the mt Bull. Mar. Sel., 22: 309-335. Polyplacc Bock, C. E., and Johnson, R. E., 1967, The rôle of behaviour in determining Chelazzi, G., the intertidal zonation of Littorina planaxis Philippi 1847 and Competiti Littorina scutulata Gould 1849, Veliger, 10: 42-54. Acanthop] Bohn, G., 1909, De l'orientation chez les patelles, C. R. Acad. Sci., Ecol. Soc 148: 868-870. Chelazzi, G., Bousfield, J. D. , Tait, A. I., Thomas, J. D., and Towner-Jones, D., and trail 1981, Behavioural studies on the nature of stimuli responsible for in the fi triggering mucus trail tracking by Biomphalaria glabrata, Malacol. Chelazzi, G., Rev., 14: 49-64. modificar Boyle, P. R., 1977, The physiology and behaviour of chitons (Mollusca: Polyplacc Polyplacophora), Oceanogr. Mar. Biol. Ann. Rev., 15: 461-509. Chelazzi, G., Brnnch, G. M., 1971, The ecology of Patella L. from the Cape Peninsula, shore and South Africa. 1. Zonation, movements and feeding, Zool • Af r. , 6: 1-38. textills hranch, G. M., 1975a, Intraspecific compétition in Patella cochlear S.), 8 (S Born, J. Anim. Ecol., 44: 263-282. Chelazzi, G., Branch, G. M., 1975b, Mechanisms reducing intraspecific compétition in Visual eu Patella spp.: migration, differentiation and territorial behaviour, Atoll, _Ji Anim. Ecol., 44: 575-600. Chelazzi, G., Branch, G. M., 1979, Aggression by limpets against invertebrate predators, ecology G Anim. Behav., 27: 408-410. Cockroft, V. G Branch, G. M., 1981, The biology of limpets: physical factors, energy •nangrove flow and ecological interactions, Oceanogr. Mar. Biol. Ann. Rev., 19: Cerithiid 235-379. Cook, S. B., 1 Branch, G. M., and Branch, M. L., 1981, Expérimental analysis of Anim. Beh intraspecific compétition in an intertidal gastropod, Littorina Cook, S. B., 1 unifasciata, Aust. J. Mar. Freshwat. Res., 32: 573-589. alternata Bree, P. J. H., 1959, Homing-gedrag van Patella vulgata L., Kon. Ned. AkadJ ..Cook, A., Bamf Wetensch., Versl. Gewone Vergd. Afd. Natuurk., 68: 106-108. _^ study on I Breen, P. A., 1971, Homing behavior and population régulation in the ^Cook, S. B., a limpet Acmaea (Collisella) digitalis, Veliger, 14: 177-183. response Breen, P. A., 1972, Seasonal migration and population régulation in the Physlol.. limpet Acmaea (Collisella) digitalis, Veliger, 15: 133-141. f Cook, S. B., a Bretz, D. D., and Dimock, R. V., 1983, Behaviorally important pulmonate characteristics of the mucous trail of the marine gastropod Ilyanassa (Say), obsoleta (Say), J. Exp. Mar. Biol. Ecol., 71: 181-191. Cook, S. B., ai Brown, A. C, 1982, The biology of sandy-beach whelks of the genus populatioi Bullia (Nassaridae), Oceanogr. Mar. Biol. Ann. Rev., 20: 309-361. interval, Brown, F., 1963, How animais respond to magnetism, Discovery, 24: 18-22. Cralg, p. c., Acmaea pe. Burke, W. R., 1964, Chemoreception by Tegula funebralis, Veliger, 6 Creese, R. G., (Suppl.): 17-20. populatloi Byers, B. A., and Mitton, J. B., 1981, Habitat choice in the intertidal Woods), 0(

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