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722 Activity Rhythms and Orientation in Sandhoppers [Frontiers in Bioscience 8, s722-732, May 1, 2003] ACTIVITY RHYTHMS AND ORIENTATION IN SANDHOPPERS (CRUSTACEA, AMPHIPODA) Alberto Ugolini Dipartimento di Biologia Animale e Genetica, Università di Firenze, Italy TABLE OF CONTENTS 1. Abstract 2 Introduction 3 Locomotor activity rhythms 4 Clock-controlled orientation 4.1. The sun compass 4.2. Modality of compensation for the apparent motion of the sun 4.3. The moon compass 4.4. Relationship between the sun and moon compasses 5 Conclusions and perspectives 6 Acknowledgements 7 References 1. ABSTRACT The aim of the present review is to combine the sandy and rocky littoral environments are ecotones in knowledge of locomotor activity rhythms with that of which periodic and non-periodic factors of biotic and compass orientation in littoral arthropods. Talitrid abiotic stress are particularly strong, so much so that they amphipods (the sandhoppers) represent a good biological condition and modulate many of the physiological and model in the fields of animal orientation and biological behavioural activities of organisms (see 1-4). The rhythms. distribution of these stress factors is certainly more intense along the Y axis: tidal alternation, waves, arrival of The paper examines the activity rhythms of predators, and variations of temperature, salinity and different species of sandhoppers (mainly Talitrus saltator), oxygen are some of the main factors acting on littoral as well as the chronometric mechanisms of compensation organisms. Some organisms tend to remain in the for the apparent motion of the sun and moon that these ecologically advantageous zone without moving animals use in zonal recovery based on the two horizontally, mainly using physiological compensation astronomical cues. The two chronometric mechanisms mechanisms. Others need to maintain a certain spatial seem to be independent of each other and to operate position that preserves stable ecological characteristics. throughout the 24-hour period. The speed of the Thus they perform excursions along the Y axis of the shore chronometric mechanism of solar compensation appears to in phase with the alternation of periodic stress factors or in be related to the hours of light and is entrained by the same relation to non-periodic factors. stimulus (light-dark alternation) that controls the circadian activity rhythm. Therefore, it is probable that in T. saltator Many studies concern the presence and function the same mechanism regulates both the circadian locomotor of locomotor activities with various types of periodicity activity and the solar compensation. (daily, circadian, tidal, lunar, circalunidian, etc.) which anticipate stressful environmental changes (for a review, 2. INTRODUCTION see 5-8). Many others deal with the identification of orientation factors and the mechanisms used during homing The littoral environment is inhabited by many or zonal recovery (see 9-12). Littoral arthropods, e.g. crabs forms of arthropods, each characterized by particular eco- of the genera Carcinus and Uca (5, 13), as well as various physiological requirements. Their spatial and temporal species of isopods and amphipods (6, 14-18), represent distribution has been investigated at the population level, classic examples of these types of studies. Therefore, although the studies are not very numerous. The littoral another review of this topic would seem to be of little environment, especially a sandy beach, is largely interest. Instead, the relationship in littoral arthropods characterized by a two-dimensional space, easily between the biological clock controlling the periodic cycle represented by two Cartesian axes: the X axis, of locomotor activity and the mechanism of chronometric corresponding to the shoreline, and the Y axis, compensation for the astronomical orientation references corresponding to the sea-land direction. Numerous factors has long been neglected. The purpose of this review is to characterize the littoral environment and are often present briefly examine the current knowledge about rhythmic in an intensity gradient, especially along the Y axis; they locomotor activity and then to devote more attention to the act differently, but constantly, on all the organisms. Indeed, orientation ability and use of astronomical orientation 722 Activity rhythms and orientation in sandhoppers Figure 1. Locomotor activity rhythm of T. saltator adults. A, in constant conditions for 50 days (sample size = 50). Abscissa, hours of the day; ordinate, time in days. The gray area indicates the period of activity of the individuals in free running conditions (from 35 modified). The insets show the activity of sandhoppers the first and the last day of experiment. B, relationship between variation of the hour of dawn and dusk during the year and the phase-shift in locomotor activity. The limits of the gray area indicate the beginning and end of the activity. SR, sunrise, SS, sunset (from 37 modified). C, semilunar locomotor activity rhythm. On the abscissa, time expressed as lunar phases; on the ordinate, total daily locomotor activity (from 39 modified). factors in a group of crustaceans, the talitrid amphipods; a few meters toward the sea to forage in the intertidal zone, they are not only highly representative of the sandy littoral although the migration is reduced or absent in conditions of environment, but also constitute an excellent biological high tide or abundant food in the wet zone (21, 30-32). The model for various types of studies. extensive study of sandhopper activity rhythms by Bregazzi and Naylor (30, also see 6) conducted in constant 3. LOCOMOTOR ACTIVITY RHYTHMS conditions clearly showed an endogenous circadian rhythm with nocturnal periodicity in T. saltator. It is regulated by It has been known for a long time that the light-dark alternation and is independent of the tidal supralittoral amphipods are mainly nocturnal animals (19- rhythm. Temperature variations within the natural range do 22). However, the first quantitative (albeit preliminary) not alter the function of the mechanism, although Pardi and laboratory investigation of the locomotor activity cycle in Grassi (33) and Bregazzi (34) found that prolonged Talitrus saltator and Talorchestia deshayesii was exposure to low temperatures (2- 6°C) could influence the conducted by Ercolini (23). In field studies using fall-traps chronometric mechanism of solar orientation and positioned at various distances from the shoreline, Geppetti locomotor activity. More recently, Williams (35) showed and Tongiorgi (24) showed that T. saltator in Italy emerges that in constant conditions (free running activity rhythm) at the surface of the wet band of sand near the water at the activity period of T. saltator remains very stable for sunset and performs landward migrations perpendicular to many days (up to 50, figure 1A) and that the photoperiod, the shore to feed at night. The length of the migration (from particularly dawn (36), is the main factor of locomotor a few tens of meters to more than 100) seems to depend activity synchronization: in the laboratory, the phase of the mainly on the environmental humidity and temperature of rhythm only changes in relation to the shifting hour of the sand. This has largely been confirmed in recent studies dawn (figure 1B). The circadian rhythm of locomotor (25-28). The return migration begins at the first light of activity varies during the year; in fact, the peak of dawn and ends in the early hours of the morning. Young locomotor activity presents a constant phase-angle individuals show a spatially reduced activity with respect to relationship with the hour of dawn (36, 37). Moreover, adults in T. saltator, and in Orchestoidea tuberculata also dawn is recognized as such by T. saltator, albeit with some the phasing of activity differs in juveniles and adults (24, individual variability, by an irradiance level of around 1-10 29). Non-periodic factors, like rain or strong waves, can lux (36 , also see 38) independently of the duration of induce diurnal activity in sandhoppers. However, in regions twilight. Yet this probably cannot be generalized to all with strong tides, T. saltator and other sandhoppers migrate sandhoppers, since the entraining stimulus for Talorchestia 723 Activity rhythms and orientation in sandhoppers the sea if partially dehydrated, toward land if in water, figure 3A), and a chronometric part that allows variation of the angle of orientation with respect to the sun during the day, thus theoretically maintaining the ecologically effective direction (chronometric photomenotaxis). Figure 3B-E shows the results of releases in a confined environment (a transparent plexiglas bowl, see 48, for details). It is evident that individuals allowed vision only of the sky and sun maintained a virtually constant mean direction independently of the hour of the release (figure 3B, C). As shown by Papi (49) and Pardi and Grassi (33), if we subject the sandhoppers to a light:dark rhythm corresponding to the natural one in duration but clock- shifted by several hours (figure 3D), we will obtain a corresponding deflection of their orientation. Figure 3E illustrates that individuals subjected to a L:D = 12:12 rhythm of artificial illumination for 1 week, anticipated by 6 hrs with respect to the natural one, showed a deflection Figure 2. Circadian variation in the scototactic response of toward the theoretically expected direction of 114°, thus T. saltator. Releases in an arena equipped with a black very near to the 90° expected on the basis of the number of screen occupying 60° of the horizon. On the abscissa, hours hours of clock-shifting and the season in which the of the day; on the ordinates, length of the mean vector of experiment was conducted. An experiment in which each release. N, noon; M, midnight; SR, subjective sunrise. individuals of the same italian population were released in The dashed line indicates the limit of statistical significance Italy and in Argentina (49) showed that the ability to (P<0.05) for each release (from 43 modified). compensate for the apparent movement of the sun is not based on local references. It should be noted that the ability deshayesii seems to be dusk (cf 37).
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