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Revista Chilcna de Historia Natural 69: 553-563, 1996 Orientation and migration in Talitrus saltator
Orientación y migraci6n en Talitrus saltator
FELICITA SCAPINI, MARIO FALLACI and MARCO C. MEZZETTI
Dipartimento di Biologia animalc e Genetica. Universita di Firenze. via Romana 17,50125 Firenze. ltalia E-mail: scapini @dbag.unifi.it
ABSTRACT
Talitrus saltator a beach dwelling crustacean amphipod, has been for long the subject of orientation studies. as it shows orientation perpendicular to the shoreline in response to stressful factors of environmental dryness or submersion. Sun orienta- tion permits zonal recovery in case of abrupt displacement from their burrows during the day, and is inherited with genetic differences among populations from differently oriented shores. Moreover, other orientation mechanisms are used in addition to or instead of the sun compass to maintain zonation. A learning capability has also been shown. which can modify the orientation after individual experience. Rhythmic components in the orientational responses have been demonstrated. which would be related to daily migrations in nature. In the laboratory under constant conditions. sandhoppers show rhythmic changes in their responses to simple \'isual stimuli and differences have been shown among populations from Mediterranean and Atlantic shores. A study is also presented aimed at answering the still open question of whether and how sandhoppers are oriented in nature during the foraging movements. which they perform at night under suitable meteorological conditions. Spontaneously active sandhoppers were captured with pit-fall cross traps positioned on the eulittoral and shortly after tested in orientation arenas. Changes in sandhopper orientation resulted during the night. which were related to their zonation and activity. The orientational cues were \isual. to both sky and landscape factors. On the whole. the results throw new light on the ecological meaning of sandhoppers orientation and the conditions in which learning of direction finding may occur in nature. Ke)· words: Talitrus saltatorethoccology. orientation. rhythms. genetics.
RESUMEN
Talitrus saltator crustáceo anfipodo cuya residencia habitual son las playas de arena. ha sido por largo tiempo objeto de cstudios de orientación debido a que se orienta pcrpendicularmente a la orilla del mar en respuesta a factores de estrés tales como desecación del ambiente o inmersi6n por efccto del oleaje. Durante cl dia la orientaci6n solar le perrnite efectuar la recuperación zonal en cl caso de un repentino traslado del área habitual de cntcrramiento. Este mecanismo de orientaci6n se hereda y prescnta diferencias geneticas entre poblaciones provenientes de playas con distintas orientaciones. Se presentan ademásotros mccanismos de orientaci6n en adici6n o en vez de la orientaci6n solar para mantener la zonaci6n. Tambien se ha cornprohado una capacidad de aprendizaje que puede modificar la orientaci6n como consecuencia de la experiencia individual. SL· ha dcmonsrrado la existencia de componentes ritrnicos en las respucstas de orientaci6n que podrian relacionarse con las migracioncs diarias ocurrentes en la playa. Bajo condiciones constantes de laboratorio, Ios anfipodos mucstran cambios rítmicos en sus rcspuestas a estimulos visuales simples. habiendose demostrado diferencias entre poblaciones costeras del Mediterráneo ) del Atlántico. El presente es un estudio que aspira a dar una respuesta a la pregunta aún abierta sobre la posihilidad y modo de orientaci6n de Ios anfipodos durante su busqueda de alimento. actividad que efectuan de noche cuando las condicioncs meteornl6gicas son apropiadas. Se capturaron anfipodos con trampas ubicadas a ras de la arena para luego ser cstudiados en cámaras de orientaci6n. Los camhios de orientaci6n que Ios talitridos manifestaron durante la noche se relaciona- ron con la zonaci6n y el estado de actividad. Las referencias para la orientación fueron visuales. cielo y paisaje. En sintesis. Ios resultados entregan nuevos antecedentes sobre el significado ecol6gico de la orientaci6n de Ios anfipodos talitridos y de las condiciones en las cuales el aprendiLaje para recuperar una dirccci6n podrfa darse en la naturaleza. Palabras clave: Talitrussaltatoretoccologia, orientaci6n. ritmos. genetica.
INTRODUCTION stage and juveniles are released from the brood-pouch of the female at an adult-like The sandhopper Ta!itrus saltator (Montagu) autonomous stage. Their typical habitat is the is a sandy-beach dweller very common on eulittoral above the high tide marks, with Mediterranean and European Atlantic coasts. slight differences in the zonation of activity Its life style is roughly the same during its between adults and juveniles, being juveniles entire life cycle; it develops without larval more active at water's edge. The research
(Received I December 1994; accepted 28 July 1996) 554 SCAPINI ET AL. done on this spec1es has revealed many directional light, substrate slope, earth's interesting points that make it a case-study, magnetic field) or to two cues in opposition. particularly for orientation and the genetic Tests have been repeated at different times of determination of orientation. We shall here day. present a brief review of this research con- The genetics of sun orientation has been sidering the many aspects of eco-ethology of studied by testing the inexperienced proge- the species, highlighting new findings that nies of different populations, reared in the await further clarification, namely the tim- laboratory under artificial light conditions; ing and plasticity of orientation behaviour. the learning capability by comparing the A field study and laboratory tests were orientation of individuals from the same performed in order to investigate how and to population which had had different ex- what extent the behaviour of sandhoppers periences (in the rearing containers or in is plastic, i.e. susceptible to both short term previous tests). modifications by changing external condi- The genetic structure of natural popu- tions and/or internal factors, and to long Iations has been analyzed with isoenzyme term ones as far as endogenous inheritable electrophoresis and a dendrogram has been information is concerned. This latter would calculated based on UPGMA clustering of be the basis of populations' adaptation and genetic distance coefficients (Nei). diversity. Spontaneous activity and migration in nature, its timing and zonation have been studied from the captures of sandhoppers in MATERIAL AND METHODS cross pit-fall traps positioned along a transect in the eulittoral zone of the beach. The traps The experiments reported in the paper have have been controlled hourly throughout a been conducted on talitrid amphipods of the 24 hour cycle, or every 2 hours for a period species Talitms sa/rotor (Montagu) from of 72 consecutive hours and repeating the Mediterranean (Italy, Fig. I) and eastern survey each month for one year. Climatic Atlantic (France, Wales) populations. To test and microclimatic conditions have been the orientation of sandhoppers the follow- registered simultaneously. ing methods have been used: I) releases in a Statistical analysis of the circular distribu- glass bowl, 40 cm in diameter, according to tions has been performed according to Pardi & Papi (I 953), in which the sandhop- Batschelet ( 1981 ). Linear simple and multiple per directional choises have been photo- regression analyses have been applied to the graphically recorded from underneath at data (Statgraphics 5.0, 1991 STSC Inc.). given intervals of time, when they hopped and crawled in the bowl; 2) releases from the centre of a circular arena, 40 cm in diameter, RESULTS and captures with pit-fall traps positioned at its rim, underlying 5° each. This method was Orientation in sandhoppers first introduced by Hartwick ( 1976) and modified by Scapini & Pardi ( 1979) to test When a sandhopper is transferred from its sandhoppers singly; 3) releases on sand and burrow to arid conditions, it runs or hops recording of the path of each sandhopper by seawards, while, when immersed in seawater using the marks of the hops. or released on a water saturated substrate, Orientation tests were performed on the it crawls or runs landwards (Scapini 1979). beach 1) with all cues available, 2) by exclud- This behaviour has been defined as zonal ing single cues (landscape vision, beach recovery. Sandhoppers have at their disposal slope) and 3) by putting cues in opposition, an abundance of mechanisms to maintain after transferring sandhoppers to a differently zonation by orienting along the sea-land axis, oriented shore. Laboratory experiments have as reviewed by Pardi & Scapini (1987). The been carried out in controlled conditions, in importance of astronomical cues, such as the order to test orientation to a single cue (sun, sun and moon azimuths and the pattern of black boundary at the horizon, artificial polarization of the light of the sky, were first ECO-ETHOLOGY OF SANDHOPPERS 555
Fig. 1: Localities on the Italian coasts where the Tulitrus saltator populations mentioned in the following figures were caught. SRO-San Rossore (Pisa); CAS-Castiglione della Pescaia, BAL-Bocca t.l"Albegna, GIA-Giannella, FEN-Feniglia, BUR-Burano (Grosseto); NET-Nettuno (Latina); BRU- Brussa (Venezia); GOR-Goro (Ferrara); TFA-Torre Fantine, LES-Lesina, ROD-Rodi Garganico, SIP- Siponto (Foggia). At SRO and FEN. two or three points were sampled. Localidades de la costa italiana donde se recolectaron poblaciones de Talitrus salllltor. SRO-San Rossore (Pisa); CAS- Castiglione ddla Pcscaia. BAL-Bocca d' Albegna. GIA-Giannella. FEN-Feniglia. BUR-Burano (Grosseto); NET-Nettuno (Lati- na): BRU-Brussa (Venaia); GOR-Goro (Fcrrara): TFA-Torre Fantine. LES-Lesina. ROD-Rodi Garganico, SIP-Siponto (Foggia). En SRO y FEN se muestrearon dos o tres puntos. demonstrated by Pardi & Papi ( 1953). How- land, according to the dryness/moisture of ever, also landscape cues, such as the dune the substrate. With experiments of boundary (Williamson 1951; 1954; Karlbrink displacement of individuals to beaches 1969; U golini et al. 1986), the differences in differently oriented from the original one, it the sky's radiance over land and sea resulting was demonstrated that astronomic orientation in different colour composition (Ercolini et generally prevails over local cues (Pardi & al. 1983 ), the earth's magnetic field (van Papi 1953; Ercolini et al. 1983). However, den Bercken et al. 1969; Arendse 1978), and different populations behave differently in the slope of the beach (Craig 1973 for this context, some of them being more tied to Orchestoidea conziculata; Ercolini & Scapini local cues than to astronomical ones (Ugolini 1974. forT. saltator) may direct the course et al. 1986). When sandhoppers are tested on of sandhoppers also in overcast conditions. a beach differently oriented from their home The wind may also direct sandhoppers as beach, they may refer to local cues they show anemonegative taxis (Papi & (landscape vision) (Fig. 2 B) or still to the Pardi 1953; Scapini et al. 1988). When the astronomical reference (sun) as on the home sun is visible these references favour a more beach (Fig. 2 D). According to Hartwick precise orientation towards the sea or the ( 1976), Orchestoidea corniculata from 556 SCAP!Nl ET AL. HOME SEA ALIEN SEA
z 0 ~ ::::> D oD-
Fig. 2: Experiment of displacement to a differently oriented shore of Talitrus saltator from the GIA-shore with the sea at 285° and the FEN-shore with the sea at 160°. Tests in orientation chamber with view of sun, sky and landscape. A: GIA- population tested at GIA-beach; B: GIA-population tested at FEN-beach; C: FEN- population tested at FEN-beach; D: FEN-population tested at GIA-beach. Points, orientation angles of individuals; anows, mean vectors of the populations; black triangles, home sea direction; white triangles, direction of the sea at the release site; u, V test with its probability; comparisons between distributions, Watson's U- square test. The tests were carried out on May 31 and June 30, 1978. (Ugolini et al. 1986, modified) Experimentos de desplazamiento de To/itrus solwtor desde las playas de origen de GIA con el mar a 285° y FEN con el mar a 160° a una play a de diferente orientaci6n. Pruebas en camara de orientaci6n con 'ista del wL cielo y paisaje. A: poblaci6n de GIA estudiada en la playa GIA: B: poblaci6n de GJA estudiada en la playa FEN: C: poblaci6n de FEN estudiada en la playa FEN: D: poblaci6n de FEN estudiada en la playa GIA. Puntos: ringulos de orientaci6n de Ios individuos: flechas: vectores medios de !as poblaciones: triangulos negros: direccion del mar en el sitio de origen de Ios anffpodos: tri~ingulos blancos: direcci6n del mar donde se liheraron Ios talitridos: u. test V con sus probabilida- des. comparaciones entre distribuciones. test U' de Watson. Los experimentos se realizaron entre el 31 de mayo y 30 de junio de 1978 (modificado de Ugolini et al. 1986).
Californian populations show a plasticity in which would explain the divergent results in the use of these orientation mechanisms. orientation tests between populations. They are oriented to landscape cues instead of the sun, in dependence of the conspi- Genetic control of orientation cuousness of landmarks on the horizon. An alternative hypothesis, which is dealt with in Sun orientation in sandhoppers is probably following section, would be to assume favoured by high selection pressure. In fact, genetic differences between populations, rapid return to the wet zone of the beach has ECG-ETHOLOGY OF SANDHOPPERS 557
survival value in cases of active or passive ~ ruco ru z displacement to dry sand, particularly when 300 ~ ~~~ ~ ffi~~ ~ the sun is shining. The most important feature of astronomical cues is that they are reliable 250 • z'i> only if the animals reside continuously in a a:- - 0 z 200 Cll 0 particular place. Individuals caught in the >-F a: 0 150 • . 0 w wild and tested away from the seashore t(g; display a sun orientation with an escape a:O ~ ~ 100 • <( w r=0943 P
Genetic analysis carried out with isoen- genetic distance (D) zyme electrophoresis on various natural 0.48 0.36 0.24 0.12 0.00 populations sampled along the Italian coasts SRO C SRO B (Fig. I) indicates that the gene flow among CAS BAL populations is relatively low (De Matthaeis GIA Tyrrhenian group et al. I 994). Measurable differences exist FEN A FEN B among some Tyrrhenian populations even FEN C BUR with small geographic distances, while two NET BRU population groups of Talitnts saltator, one GOR LES living on the Ligurian-Tyrrhenian shores and ROD TFA the other on the Adriatic, diverge at a genetic Adriatic group SIP distance of 0.4 (Fig. 4). Genetic heterogenity was also shown to rig. -1: Dendrogram of Talitrus saltator popula- exist within natural populations when the tions based on UPGMA clustering of genetic orientation performances of the progenies distance coefficients (Nei) calculated from an of different pairs were compared (Scapini allozymic study on 19 loci. The localities are & Buiatti 1985; Scapini et al. 1989). The shown in Fig. I. (De Matthaeis et al. 1994, variances within each family were smaller modified). than those among the various families. The Dendrograma de poblaciones de Talitrtts saltator basado en intra-population heterogenity would favour el agrupamiento UPGMA de coeficientes de distancia gene- tica (Nei) calculados en estudio alozimico de 19 locus. Las long term adaptation to a changing environ- poblaciones son las mismas indicadas en la Fig. I. (Modifi- ment. cado de De Matthaeis et al. 1994). 558 SCAPINI ET AL.
Flexibility of orientation present a black/white boundary on the ho- rizon (Scapini et al. 1993). On the other hand, a merely inherited sun orientation without control and/or compensa- Migration in nature, its timing and control tion mechanisms would be too rigid a behav- The timing of spontaneous moveme~ts ~n iour and not really adaptive in a highly varia- the beach, their zonation and the climatic ble environment such as a sandy shore conditions in which movements occur have (Hazlett 1988). Sandy beaches are subject- been studied on a beach-dune system of the ed to periodic and aperiodic actions by wind, Tuscan coast (Scapini et al. 1992). It has waves and currents, which may well change been shown that sandhoppers emerge the direction of shorelines even on a rel- spontaneously after sunset and burrow into atively short time scale in relation to the the sand again during the first hours of the Iifespan and generation rate of sandhoppers day (Fig. 6). A similar rhythm of activity has (McLachlan 1988). Both from laboratory been shown to be endogenous in the labora- rearing and a survey in the field, evidence tory under constant conditions on Atlantic has been found that T. saltator on the Medi- sandhoppers by Bregazzi & Naylor (1972) terranean coast can survive more than one and Williams (1983). But in nature there year, with a maximum of two years, while were seasonal differences in this rhythm as three months are needed to develop to the well as differences between adult and young adult stage (Scapini, unpublished data). individuals (Fig. 6, A, B). Moreover, limited Thus, in the course of their life sandhoppers activity during the day was in some condi- may well be obliged to change their inbo~n sun orientation according to local changes m BEFORE AFTER 10 TRIALS the shoreline direction, as well as in case of accidental displacement to a differently oriented shore. Evidence that learning a new LABORATORY direction occurs in nature can be seen in BORN sandhoppers living on a lagoon shore almo.st opposite to the seashore: adults collected m the field and tested with the vision of the sun, 00 oriented according to the lagoon shore, while their laboratory-born offspring directed seawards (U golini & Scapini 1988). A modi- WILD fication of orientation was obtained by rear- CAUGHT ing sandhoppers from the seashore in en- closures positioned on the lagoon-shore opposite to it (Ugolini et al. 1988). Scapini et Fir.:. 5: Sun orientation of Talitrus saltator before al. ( 1988) succeeded in training individual and after I 0 training trials within a tube oriented adult sandhoppers to orient in a direction dif- at 120° from the home sea direction. CAS pop- ferent from the inborn one (Fig. 5). ulation tested in Florence. Points, directions Other orientation mechanisms, response chosen by the individuals in the test arena; arrows, mean vectors of the samples with their to slope, to a black/white boundary above the confidence limits for P = 0.05; triangles, home horizon and magnetic compass, have been sea direction; double lines inside the circles, tube shown to be inborn, but also subjected to mo- position during the training. (Scapini et al. 1988, dification according to experience. In some modified). pr~sent populations a magnetic compass. is. Orientaci6n solar de Talitrus saltator. antes y despues de l 0 in laboratory-born individuals while It disap- pruebas de adiestramiento dentro de un tubo orientado en pears in experienced wild-caught individua!s 120° con respecto a la posici6n del mar en el lugar de on- gen (poblaci6n CAS estudiada en Florencia). Puntos: direc- (Scapini & Quochi 1992). The scototactic ciones elegidas por Ios individuos en la arena expe;unental; response towards a black shape is also more tlechas: vectores medios de !as muestras con sus !mutes de evident in young individuals than in adult confianza para P = 0.05; triangulos: direcci6n del mar en e]]uo-ar de orio-en: lfneas dobles dentro de Ios cfrculos: post- ones, and the response can be modified by cion del tubo durante el adiestramiento. (Modificado de Sca- rearing sandhoppers in containers that pini et al. 1988). ECG-ETHOLOGY OF SANDHOPPERS 559 A April 10-13, 1986 •c RH 70 100 --~ul~ n- ~at11e -----· wen r.. n-756 r • humldl~ go ,... 60 _.. ...- ...... ~ , 40 80 li' 50 / -- \ 70 ' ~.,.,..--_ i 40 ------30 60 f 50 .t: 30 • 20 40 li 20 ····· 30 8- 10 20 .. 10 10 0 0 0
12 14 16 18 20 22 24 2 4 6 8 10 12 hoc.ra B August 19-22, 1986 •c RH 70 50 100 - adulta n-148 t.Tat11e g60 -----· jwenllea n- 13 _, rei • humidity go ...... 0 80 l;-50 ,., ...- --- 70 / - 40 ' '-- JO 60 !er ···················--...... ··········· 50 : 30 .. 20 40 i 20 30 .. 10 10 20 10 0 0 0 12 14. 16 18 20 22 24 2 4 6 8 10 12 houra Fig. 6: Surface activity along the day of adult (continuous lines) and juveniles (broken lines) Talitrus saltator on the BUR beach, from capture rates with pit-fall traps. Air temperature and relative humid- ity arc reported. n: total number of sandhoppers in the traps. (Scapini et al. 1992. modified). Actividad diurna en superficie de adultos (lfneas continuas) y juveniles (lfneas discontinuas) de Ta/itrus .w!tator en la playa BUR. Estirnaciones obtenidas de captu- ras con uso de trampas colocadas a ras del suelo. Se grafica tambien la temperatura y humedad relativa. n: numero total de anffpodos en !as trampas (Modificado de Sca- pini et al. I 992).
tions apparent on the Mediterranean, while was an inhibiting factor in summer and on the Atlantic and Baltic it has been exclud- autumn, while it favoured activity in spring; ed for the adults (Karlbrink 1969) but not for air humidity and rain generally favoured the juveniles (Rlippel 1967). activity, while air pressure was positively A multiple regression analysis of surface correlated with activity in winter but activity with various climatic and micro- negatively in summer. Moreover, the activity climatic parameters reveals that in nature of young sandhoppers of a size up to 5 mm activity is modulated by external conditions. seems to be more linked to relative air hu- The surface activity of adult sandhoppers midity and to wind speed than it is in adults. turned out to be significantly correlated with Orientation of spontaneous activity air and sand temperature and humidity, air pressure, wind or rain. The picture changes Another question was whether the spontan- at different times of the year as might be eous movements of the animals were also expected. For example, high air temperature oriented during active migrations. In general 560 SCAPINI ET AL. landward migration occurred in the early sponse, which favour zonal recovery or drift hours of the night, later and in daylight be- at the appropriate time. Edwards & Naylor coming seaward (Scapini et al. 1992). The (1987) tested an Atlantic population of Tali- landward migration might be seen as a pas- trus saltator under constant laboratory sive flux or drift, conditions at the water·~ conditions for its response to black/white edge being limiting; in fact sandhoppers d(' h, 'll JHiary on the horizon, and obtained a retreat from water (Scapini 1979). How- A ever, this might also be an active orientation * {P<005Rayle,ghtest) directed by environmental cues. 08
Aiming at understanding if sandhoppers' *n=20 06 * n=101* spontaneous movements are oriented and n=48 which orienting factors, astronomical and/or 04 n.. 42 landscape cues, are actually used by the 02 animals, we tested sandhoppers in two circu- n,26 lar arenas positioned on the sand, one of 23 00 24 00 01.00 02.00 0300 0400 0500 0600 0700 which screened the view of the landscape, TIME while both permitted a complete view of the B * (P clear orientation toward the boundary during SR ss 0.7 the day with scattering at night. By way of ~ SR ~ ss ~Atlantic •HH Mediterrcnecl'1 "0 contrast, a response away from the boundary c M :;;,"' at night, with scattering during the day, was .8 I \ 0.3 obtained with a Mediterranean population "E I .!!., ~ I ' B"' _-;,.- ~ -;_: :2.-- ______-:'~ ____ --,F:;;' :.-; ::.- P-Oos (Fig. 8; Mezzetti et al. 1994). 0.1 6 ' ..L _ f ------\ _ ....L --- A rhythmic responsiveness of Mediterra- I \ I \ nean sandhoppers was also shown in the ____ .... ·, / 'i.-j ...... r • ~ ------J_ ------\---- PeQ,Q5 laboratory with respect to a directional light, I with one peak at night when a blue light was used, and two peaks at dawn and at sunset with a yellow light (Fig. 9 A). A similar drop 0900 1200 1500 1600 of response around the middle of the night Time of day was apparent in nature with the full moon, as Fig. 8: Rhythm of orientation of Talitrus saltator stressed above (Fig. 7). Again, this behaviour from a British Atlantic, Newborough Anglesey, contrasts with the orientation of a French (triangles) and the Mediterranean BUR (squares) populations with respect to a black/white Atlantic population (Fig. 9 B), which was boundary on the horizon. Tests were conducted photopositive at night and photonegative in the laboratory under continuous light condi- during the day (Mezzetti et al. 1994). tions. SR: subjective sunrise; SS: subjective These differences in behaviour among sunset; P: probability levels for the Rayleigh test. populations can be explained by the different Each symbol represents the mean vector length of ecological pressures, as was stressed by one sample. (Mezzetti et al. 1994, modified). Mezzetti et al. ( I 994 ), who compared Atlantic Ritmo de orientaci6n de Ta!irrus saltator en una poblaci6n and Mediterranean populations subjected to Atiantica Britanica. Newborough Angie;,ey (triangulos) y different tidal regimes. On the Mediterranean una Mediterranea (piaya BUR. cuadrados) en relaci6n a un lfmite negro/blanco en el horizonte. Los experimentos se coasts the highest risk apparently is dehydra- realizaron en el laboratorio bajo condiciones de luz conti- tion, thus a rapid seaward zonal recovery has nua. SR: amanecer subjctivo, SS: atardecer subjetivo: P: ni- a higher survival value, while on the Atlantic veles de probabilidad para el test de Rayleigh. Cada sfmbolo rcpresenta la longitud del vector media de una muestra (mo- tidal shores the risk of being washed away dificado de Mezzetti et al. 1994). favours landward orientation at dawn from the feeding zone between high and low tide marks. complex of environmental stimuli typical of a particular beach, which may change periodically and aperiodically. At birth a DISCUSSION sandhopper has a set of simple behaviours at its disposal, such as biological clocks and On the whole we have here a picture of a different taxes: orientation to slope, earth's very plastic behaviour, which can be finely magnetic field, sun, moon, polarized light, modulated on the individual level as the en- dune contour, brightness of the sea. These vironment changes. Moreover, adaptive innate responses have been experimentally modifications can be fixed in the gene-pool demonstrated at least for some populations. on a population level, as demonstrated by Experience with one particular environment both the behavioural (orientation and rhythms may induce an integrated response to the of responsiveness) and molecular (isoen- complex of environmental stimuli, different zymes) differences recorded among the pop- for different localities. For example, in one ulations. locality, with an obvious dune and a sloped We can now propose a model which sug- beach, orientation to landscape and slope gests how differences could rapidly emerge may become particularly important, together and be fixed as heritable mechanisms in po- with a coupling of the circadian clock with pulations living on beaches subjected to dif- the sun-sky polarization movement. Moon ferent ecological pressures. As we have and magnetic orientation would be useless in already pointed out, sandhoppers in nature such conditions and therefore inoperative. In integrate and opportunistically respond to a contrast, in another environment, landscape 562 SCAPINI ET AL. SR ss The new generation would inherit all the A 1.0 J simple behaviours and select among them the adaptive complex according to its expe- 0.8 rience. But, in particular cases regarding A relatively stable beaches, it might also inherit .E o.e I \ g I \ a facilitation for coupling some adaptive 'E I \\ I taxes, in the form of regulatory genes. Pre- 'z,. / ~ 0.4 ' / -- ~- -- - - P=0.01 vious research on the inheritance of the sun ------• Pc0.05 orientation directional tendency in Medi- 0.2 ..... 452 nm ~543 nm terranean sandhoppers has dealt with such a case. o.o -r-..~-,--.~,.....~.....-~r-r~r-r~....-...,...,~.,...... , 0000 0300 0600 0900 1200 1500 1800 2100 2400 The differences in timing of the orienta- Time of day tional responses to different visual stimuli which were shown in Atlantic and Medi- B terranean populations might be inherited as 0.7 well, but this still awaits evidence, remaining .E g 0.6 a working hypothesis that should and can be 'E easily tested. j O.l 0.1 ACKNOWLEDGMENTS -0.1 E ,g The research was supported by the Centra di ~ -0.3 Studio per la Faunistica ed Ecologia Tropi- ~ ------· cali, Consiglio Nazionale delle Ricerche, -M ;-,~-,-.~.,--,.~.....-~r-r~r-r~....-..,_,~.,....., 0000 0300 0600 0900 1200 1500 1800 2100 2400 Ministero dell'Universita e della Ricerca llma of day Scientifica 40% and 60%. We wish to thank Fig. 9: Rhythm of orientation of Talitrus saltator the Italian W ordl Wildlife Found for having from the Meditenanean BUR (A) and a French allowed the experiments in the field at the Atlantic, Gran Crohot, Bordeaux, (B) population with respect to a monochromatic blue (squares) Oasi di Burano. Dr. Marcela Claudia Lagar and yellow (triangles) light. Tests were con- kindly translated the Spanish text. ducted in the laboratory under continuous light conditions. Each symbol represents the mean vector length (r) of one sample. SR: subjective LITERATURE CITED sunrise; SS: subjective sunset; P: probability levels for the Rayleigh test. (Mezzetti et al. 1994, ARENDSE MC ( 1978) Magnetic field detection is distinct modified). from light detection in the invet1ebrates Tenebrio and Talitrus. Nature 274: 358-362. Ritmo de orientacion de Tuli1rus salta!or en una poblaci6n BA TSCHELET E ( 1981) Circular statistics in biology. Mediterdnca. BUR (AJ y una Atlantica Francesa. Gran Academic Press. London. Crohot. Bordeaux. (B) con respecto a luz monocrornatica BERCKEN J VAN DEN. S BROEKHUIZEN. J RINGEL- azul (cuadrados) y arnarilla ttriangulos). Los experimentos BERG & HHW VELTHUIS (1967) Non-visual se realizaron en el laboratorio bajo condiciones de luz conti- orientation in Tali1rus sal/a/Or. Experientia 23: 44- nua. Cada simbolo indica la longitud del vector rnedio (r) de 45. una muestra. SR: arnanecer subjetivo. SS: atardeccr subjeti- BREGAZZI PK & E NA YLOR ( 1972) The locomotor vo. P: niveles de probabilidad para el test de Rayleigh. (Mo- activity rhythm of Talilrus saltator (Montagu) (Cru- dificado de Mczzetti et al. 1994). stacea, Amphipoda). Journal of Experimental Biology 57: 375-391. CRAIG PC ( 1973) Orientation of the sand-beach amphipod. and beach slope factors would be irrelevant Orclzestoidea comicu/ata. 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