Rhythmic activity responses of the fiddler crab Uca crenulata to artificial tides and artificial light

The fiddler crab Uca crenulata, from California (USA), was exposed to artificial tides in order to differentiate between the influence of a tidal cycle from that of a light-dark cycle on its locomotor activity. Most crabs could be well synchronized by tides, but the activity patterns of other crabs was merely exogenously reinforced. Under constant conditions, after tidal treatment, crabs showed bimodal or unimodal activity patterns. When a 24 h light-dark cycle and a 12.35 h tidal cycle acted as concurrent stimuli, their effectiveness in synchronizing the crabs' activity was variable, depending on the undividual. It is likely that crabs which tend to exhibit a unimodal activity pattern are more sensitive to a light stimulus, whereas crabs with a bimodal activity pattern respond preferably to the tides. Thus, responses of endogenous activity of U. crenulata to tides and light-dark cycles are similar, suggesting that the basic oscillarory mechanism for circadian and tidal activity may be the same.     

Looking for the clock mechanism responsible for circatidal behavior in the oyster Crassostrea gigas

Valve activity rhythm of the oyster Crassostrea gigas is mainly driven by tides in the field, but in the laboratory, only a circadian clock mechanism has been demonstrated. In an attempt to reconcile these results, the mechanisms underlying the circatidal rhythm were studied in the laboratory under different entrainment or free-running regimes and in the field at Arcachon (44°39′N/1°09′W) in February–April 2011). Results confirm the existence of a circadian clock in C. gigas. Under entrainment regimes (12-h dark/12-h light photoperiod and tidal cycles simulated by a reversing current flow), oysters exhibited both circadian and circatidal cycles. Under free-running conditions (e.g., continuous darkness), the endogenous rhythm appeared to be circadian. There was no experimental evidence for an endogenous circatidal rhythm, even in oysters just transferred from the field, where a clear tidal cycle was expressed. There are two possible mechanisms to explain tidal behavior in C. gigas: an exogenous tidal cue that drives tidal activity and masks the circadian rhythm and an endogenous circatidal clock that is sensitive to tidal zeitgebers and runs at tidal frequency.     

Circatidal rhythm of an intertidal crab, Hemigrapsus sanguineus : synchrony with unequal tide height and involvement of a light-response mechanism

The circatidal rhythm of intertidal animals may reflect the inequality of the tides. In addition, a light-sensitive mechanism may be involved in their internal timing systems. To test these hypotheses, the larval release activity of the intertidal crab Hemigrapsus sanguineus was monitored under different light conditions in the laboratory. Under a 24-h light–dark (LD) cycle with the phase similar to the field, the activity coincided with the times of high tide in the field and showed a tidal rhythm. This rhythm free-ran in constant, dim-light conditions, suggesting that the timing is controlled by an endogenous clock. When the population was exposed to a 24-h LD cycle with the phase changed from that in the field, the tidal rhythm was phase-shifted; while the light cycle advanced in phase from the field caused a phase-advance of the rhythm, that delayed in phase induced a phase-delay of the rhythm. Thus, a light-response mechanism is definitely involved in circatidal timing systems. But the population rhythm showed a large variability among individuals, associated with the phase-shift, and the magnitude of the phase-shift did not accurately correspond to that of the light cycle. These results suggest that the light-response system can control the phase of the rhythm less stronger than that in estuarine crabs. Most releases occurred at higher high tides, but the release of some females obviously occurred at lower high tides. The larval release pattern thus could not be accounted for by a simple synchrony with higher high tides. Hatching of H. sanguineus occurred after a “hatching program” of 49.5 to 52.5 h. This program is initiated by some factor (hatching-program inducing stumuli: HPIS) transmitted from the female to the embryos. We speculated that this factor is effectively transmitted to the embryos when the habitat is exposed to air, i.e., at lower low-tide periods, and that once each embryo is stimulated, hatching occurs synchronously 2 d later during high tide. The release of HPIS is probably controlled by the circatidal clock of the female, and the 24-h LD cycle may participate in shifting this timing to the opposite low tide. Received: 14 January 1997 / Accepted: 18 February 1997     

External synchronizers of tidal activity rhythms in the prawns Penaeus indicus and P. monodon

Phasing of persistent circatidal rhythmicity to an artificial tidal cycle was assessed in the prawns Penaeus indicus Milne Edwards and P. monodon (Fabricius) collected from the Vellar estuary, South India, in the period between June and December 1984. Simulated 6 h cycles of 20 and 30 S, and 6 h cycles of 20° and 30°C induced a persistent tidal rhythmicity after 20 cycles. The imposed 6 h cycles of 25 and 30 S, and 25° and 30°C induced tidal rhythms after 30 cycles. In both cases, re-established tidal activity rhythms were evident for at least 48 h — higher activity occurring during the higher salinity and lower temperature phases of the simulated tidal cycles. Artificial tidal cycles of still water and running water synchronized the tidal rhythm after 20 cycles. Combined 30 S, 20°C, for 6 h and 20 S and 30°C for 6 h established a persistent tidal rhythm after 10 cycles, whereas wave action had no influence on tidal synchronization. The influence of possible interactions of tidal rhythms and in situ tidal variables on circatidal activity is discussed.     

Activity rhythms of two cirolanid isopods from an exposed microtidal sandy beach in Uruguay

Activity rhythms of two cirolanid isopods, Excirolana armata and Excirolana braziliensis, were studied based on both seasonal field observations and laboratory experiments, at an exposed microtidal sandy beach in Uruguay. The natural emergence patterns of both species were observed in the field for 1 year, twice in each season, and correlated to sea level, expected tidal cycles and diel cycles. Laboratory experiments were carried out in order to detect endogenous rhythms of activity and observe how emergence of both species was affected by changes in light and/or sediment thixotropy. We also compared behavioral strategies of sympatric species that occupy different beach levels. Sea level (and thus swash zone position) during field sampling did not follow expected tidal cycles for most sampling occasions. E. armata was observed in activity most of the time, but activity only correlated with sea level on three out of eight occasions, and only once was correlated to expected tidal cycle. Laboratory results showed that emergence under constant conditions was rare; changes in sediment thixotropy stimulated emergence, but the response was not cyclical; light had little effect on this response. On the other hand, E. braziliensis was fairly scarce in the water column, but swimming individuals were observed always during the night. They displayed an endogenous circadian activity pattern in the laboratory which augmented in response to changes in sediment thixotropy. The natural light/dark cycle modulated both spontaneous and response emergence by increasing day/night differences in activity. In this study E. armata, a midlittoral species more exposed to sea level variations, seemed to rely entirely on different physical and/or biological cues to trigger emergence at the appropriate time. E. braziliensis, found mostly in the upper intertidal zone, emerged in a circadian rhythm, which was stimulated by changes in sediment thixotropy and reinforced by light cycles. The results of this study led us to conclude that on microtidal, unpredictable beaches, local physical and biological factors can combine to determine different activity strategies in organisms from different intertidal levels. Received: 23 March 2000 / Accepted: 30 August 2000     

Circatidal swimming activity rhythm in a subtidal cumacean Dimorphostylis asiatica (Crustacea)

Dimorphostylis asiatica, a cumacean crustacea inhabiting the sublittoral line of the Seto Inland Sea, shows a rhythmic pattern of swimming activity coinciding with daily and tidal components in the field. This activity pattern was bimodal at first, i.e., circatidal activity coinciding with high tides at their habitat. The mean free-running period (i.e., bitidal interval) of this endogenous rhythm was 23.1 h at 10°C, which was significantly shorter than the environmental tidal cycle. In most cases (90% of the records) this bimodal activity became unimodal within 10 d. The unimodal period was 24 to 27.5 h, which is markedly longer than the preceding bimodal period. The bimodal pattern observed in the present study was not observed in the field. The difference between field and laboratory activity patterns can be explained in terms of direct response of the bimodal circatidal rhythm to the day-night cycle in the field. Field observations were made and laboratory experiments conducted between 1988 and 1992.     

Gezeitenrhythmische Nahrungsaufnahme und Kotballenablage einer terrestrischen Milbe (Oribatei: Ameronothridae) im marinen Felslitoral

Feeding, locomotory and defecatory activity of the algivorous orbatid mite Ameronothrus marinus have been measured under defined conditions in the laboratory. Of terrestrial origin, these mites inhabit the intertidal zone of rocky shores along the North and Baltic Seas. Under daylight cycles found at the sampling site and in the absence of tides, feeding and defecation follow an endogenous rhythm with a spontaneous period of 12.3 h; in the tideless littoral of the Baltic Sea these activities are synchronized with diurnal cycles. Feeding and defecation follow a definite sequential pattern, repeated on the average every 4 h, i.e., 3 times between two high tides. The phase of this tidal feeding-defecation rhythm is determined by the onset of the high tide, and different patterns of this rhythm can be observed according to the tidal zones. Inhabitants of the lower eulittoral exposed to longer periods of submersion start feeding earlier, take up more food at one time before the beginning of high tide, quickly defecate part of the food undigested after feeding, and later produce other faecal pellets which contain the real remains of digestion. Inhabitants of the upper eulittoral, exposed to shorter periods of submersion, start feeding later and extend their feeding activity over the whole period of low tide; the difference between faecal pellets with digested and undigested contents is indistinct. The occurrence of these different types of faecal pellets in inhabitants of the intertidal zone is interpreted as a compensatory physiological adaptation resulting from increasing periods of submersion.     

Endogenous swimming rhythms in estuarine crab megalopae: implications for flood-tide transport

Up-estuary migration of crab larvae to adult habitats is thought to be accomplished by selective tidal transport in which late-stage larvae enter the water column on flood tides and remain on or near the bottom on ebb tides. This study measured endogenous rhythms in swimming by the last larval stage (megalopa) of blue crabs Callinectes sapidus and fiddler crabs Uca spp. Previous field studies found that megalopae of both species were only abundant in the estuarine water column on nocturnal rising tides. Megalopae were collected from the Newport River Estuary, North Carolina (34°41N; 76°40W) during August–September 1992 and swimming activity was recorded for 4.5 to 7 d under constant conditions with a video system. Rhythms exhibited by both genera in the laboratory were not identical to those recorded in the field. Uca spp. displayed a circatidal rhythm, with maximum swimming occurring near the time of high tide in the field. Rhythm amplitude increased when crushed oyster shells were present, which suggested that megalopae bury or cling to the substrate during quiescent periods. In contrast, C. sapidus had a circadian rhythm in which maximum swimming coincided with the day phase in the field. In most trials, the activity of blue crab megalopae was unrelated to the expected tidal cycle. It was concluded that a tidal rhythm in swimming was the behavioral basis of flood-tide transport for fiddler crab larvae. The endogenous rhythm in blue crabs does not participate in transport, which probably results from behavioral responses to environmental cues associated with flood tide.     

Circadian rhythm of swimming activity in juvenile pink salmon (Oncorhynchus gorbuscha)

The circadian rhythm of swimming activity and the role of the daily illumination cycle in the synchronization of this rhythm were studied in individual juvenile pink salmon. Sixty eight percent of all fish examined (n=38) were day-active when exposed to a 12 h L:12 h D cycle; the remaining fish were nocturnally active. One half of the fish tested under laboratory conditions of continuous, constant light intensity (LL) and constant temperature showed unambiguously endogenous activity rhythms with circadian periods for up to 10 d. The remaining fish were arrhythmic. Mean period length of the free-running activity rhythms for diurnal fish in LL shortened with constant light intensity increasing from 6 to 600 lx, as predicted by the circadian rule. In contrast, mean free-running period for nocturnal fish did not vary significantly with similarly increasing constant light intensity. Mean swimming speed (activity level) of both diurnal and nocturnal fish increased significantly with increasing light intensity. This is suggestive of a positive photokinetic response. When subjected to a phase-delayed LD cycle, the fish resynchronized their daily rhythms of activity with this new LD cycle after only one transient cycle in most instances. Hence, the timing of the daily activity rhythms appeared to occur through the direct masking action of the illumination cycle on activity, rather than through entrainment of an endogenous circadian system.     

Tidal and circadian activity rhythms in juvenile plaice,Pleuronectes platessa

Young plaice (Pleuronectes platessa L.), caught in the intertidal zone, exhibit a short-lived tidal rhythm when their activity is recorded in darkness in the laboratory. This tidal rhythm rapidly changes to one of circadian frequency both in darkness and in light-dark cycles. It is considered that the basic rhythm is circadian in nature, but that it can be entrained to keep in phase with the tides by some, as yet unknown, Zeitgeber present under tidal conditions.     

Rhythms in larval release of the sublittoral crab Neopanope sayi and the supralittoral crab Sesarma cinereum (Decapoda: Brachyura)

Ovigerous females of the subtidal xanthid crab Neopanope sayi (Smith) and the high intertidal grapsid crab Sesarma cinereum (Bosc) were collected during the summers of 1986 and 1987 in the Beaufort, North Carolina (USA), area and brought into the laboratory, where rhythms in larval release were monitored. When crabs with late-stage embryos were put under a 14 h light:10 h dark cycle in an otherwise constant-environment room, an apparent tidal rhythm in release of larvae was observed for both species, with N. sayi releasing near the time of day and night high tides, and S. cinereum releasing around the time of night high tides. The time of sunset relative to high tide was a complicating factor, since larval release for both species was often concentrated around sunset when evening high tides fell several hours before sunset. When a group of N. sayi and S. cinereum were brought into the laboratory and placed under constant lowlevel light for 5 d, the release rhythm of the population persisted, thus implying that the rhythm is endogenous. Larval release near the time of high tide and often at night is common among brachyurans living in tidal areas, regardless of specific adult habitat, suggesting a common functional advantage. Possibilities include transport of larvae from areas where predation and the likelihood of stranding and exposure to low-salinity waters are high, as well as a reduced probability of predation on adult females. Results of the present study suggest that the importance of release after darkness may increase with increasing tidal height of the adult.     

Endogenous swimming rhythms underlying the spawning migration of the blue crab, Callinectes sapidus: ontogeny and variation with ambient tidal regime

Spawning female blue crabs, Callinectes sapidus, use ebb-tide transport (ETT) to migrate seaward. In estuaries with semi-diurnal tides, ETT in ovigerous blue crabs is driven by a circatidal rhythm in vertical swimming in which crabs ascend into the water column during ebb tide. The ontogeny of this rhythm was examined by monitoring swimming behavior of females before the pubertal molt, females that had recently undergone the molt but had not yet produced a clutch of eggs, and ovigerous females from an estuary with strong semi-diurnal tides. To assess variation in swimming rhythms with ambient tidal regime, swimming rhythms of ovigerous females from semi-diurnal (Beaufort, North Carolina), diurnal (St. Andrew Bay, Florida), and non-tidal (South River, North Carolina) estuaries were compared. Experiments were conducted during the summers of 2006–2008. Female crabs prior to oviposition had variable endogenous swimming rhythms (circadian, circatidal, or circalunidian). Ovigerous females from estuaries with semi-diurnal and diurnal tides had pronounced circatidal or circalunidian rhythms with swimming during the time of ambient ebb tide. Swimming rhythms of several ovigerous crabs switched between circatidal and circalunidian during the ~5-day observation period. Ovigerous crabs from a non-tidal estuary had a circadian rhythm with vertical swimming around the time of sunset. These results suggest that, while endogenous swimming rhythms are present in some female blue crabs prior to oviposition, rapid seaward movement via ETT in tidal estuaries begins following oviposition of the first clutch of eggs.     

The effect of food availability on the semilunar courtship rhythm in the fiddler crab<Emphasis Type="Italic"> Uca lactea</Emphasis> (de Haan) (Brachyura: Ocypodidae)

Semilunar or lunar reproductive rhythms that follow tidal cycles are common in marine animals. For brachyuran crabs, an adaptive explanation for the synchronous release of larvae in phase with the tidal cycle is that females release larvae when their offspring are best able to escape predators. As a corollary to this hypothesis, the synchronous male reproductive cycle is selected to be in phase with female receptivity. As an alternative hypothesis, we propose that variation in food abundance influences the onset and intensity of the semilunar courtship cycle. We tested this hypothesis in male fiddler crabs ( Uca lactea) by experimentally manipulating food availability for 4 weeks. Food-supplemented males built more semidomes and waved for more days than did food-deprived males or untreated control males. Moreover, food-supplemented males began courtship earlier and the median courtship day advanced with an increase in food. Courtship intensity was not related to crab size. These results provide the first evidence in marine animals that changes in food abundance due to the tides, and hence in phase with the semilunar cycle, influence male reproductive rhythm.     

Effects of endogenous and some exogenous factors on the activity of the juvenile banana prawn Penaeus merguiensis

In conditions of alternating light and dark, juvenile Penaeus merguiensis de Man are more active during the dark phase. The rhythm persists in continuous dim red light, but not in continuous bright white light. The period of circadian rhythm shown in continuous dim red light varies between individuals from 22.75 to 26.0 h, with a mean of 23.8 h. The response of prawns to an artificially produced tidal situation is mediated by the presence or absence of water flow. No endogenous component of this tidal rhythm was demonstrated. There is an irregular short-term rhythm (period 2 to 3 h). It is suggested that this allows starved prawns to conserve energy.     

Circatidal swimming behavior of brachyuran crab zoea larvae: implications for ebb-tide transport

Larvae of the blue crab Callinectes sapidus and fiddler crab Uca pugilator are exported from estuaries and develop on the continental shelf. Previous studies have shown that the zoea-1 larvae of some crab species use selective tidal-stream transport (STST) to migrate from estuaries to coastal areas. The STST behavior of newly hatched larvae is characterized by upward vertical migration during ebb tide followed by a descent toward the bottom during flood. The objectives of the study were (1) to determine if newly hatched zoeae of U. pugilator and C. sapidus possess endogenous tidal rhythms in vertical migration that could underlie STST, (2) to determine if the rhythms persist in the absence of estuarine chemical cues, and (3) to characterize the photoresponses of zoeae to assess the impact of light on swimming behavior and vertical distribution. Ovigerous crabs with late-stage embryos were collected from June to August 2002 and maintained under constant laboratory conditions. Following hatching, swimming activity of zoeae was monitored in darkness for 72 h. U. pugilator zoeae displayed a circatidal rhythm in swimming with peaks in activity occurring near the expected times of ebb currents in the field. Conversely, C. sapidus zoeae exhibited no clear rhythmic migration patterns. When placed in a light field that simulated the underwater angular light distribution, C. sapidus larvae displayed a weak positive phototaxis at the highest light levels tested, while U. pugilator zoeae were unresponsive. Swimming behaviors and photoresponses of both species were not significantly influenced by the presence of chemical cues associated with offshore or estuarine water. These results are consistent with predictions based on species-specific differences in spawning and the proximity of hatching areas to the mouths of estuaries. U. pugilator larvae are released within estuaries near the adult habitat. Thus, ebb-phased STST behavior by zoeae is adaptive since it enhances export. Selective pressures for a tidal migration in C. sapidus larvae are likely weaker than for U. pugilator since ovigerous females migrate seaward prior to spawning and hatching occurs near inlets and in coastal waters.     

Social synchronization of the activity rhythms of honeybees within a colony

Colonies and isolated bees of the Cape honeybee, Apis mellifera capensis Esch., were observed for evidence of circadian rhythmicity under constant conditions. It was found that colonies develop free-running activity rhythms in self-selected light-dark cycles, which are slightly shorter than 24 h. The periods of the activity rhythms of individual isolated bees were longer than 24 h in self-selected light-dark and constant light, while they were shorter than 24 h in constant darkness. A greater variability in period was found in the isolated bees than in the colonies. When the rhythms of colonies and individual bees from these colonies were measured simultaneously, the activities of the isolated bees drifted with respect to that of the colonies, their period being either longer or shorter than that of their own colony. After 12 days of isolation of individual bees from their colony, all coincidence between the phases of the two rhythms was lost. We conclude that the periods of common activity and common rest of the bees within a colony result from a mutual (social) synchronization of the rhythms of the individual bees.     

The tidal rhythm of extracellular digestion and the response to feeding in Ostrea edulis

Under natural conditions, on the shore, there is a tidal rhythm for changes in pH, length, and protein and amylase content of the crystalline style of Ostrea edulis L. When oysters were kept immersed and fed continuously for 2 weeks, in the laboratory, the rhythm of extracellular digestion was lost. Oysters were fed discontinuously for 2 weeks, in the laboratory, with a 6 h-on, 6 h-off feeding regime. During the feeding period, the changes in pH, size, and protein content of the style were similar to the changes observed in the field over the period of high tide. It is our hypothesis that the tidal rhythm of extracellular digestion in Ostrea is not endogenous, but is controlled by feeding activity.     

Circatidal activity rhythms in ovigerous blue crabs, <Emphasis Type="Italic">Callinectes</Emphasis><Emphasis Type="Italic">sapidus</Emphasis>: implications for ebb-tide transport during the spawning migration

Female blue crabs (Callinectes sapidus Rathbun) with mature embryos have a spawning migration in which they: (1) undergo ebb-tide transport for movement seaward from estuaries, (2) release their larvae, and (3) reverse direction by undergoing flood-tide transport for up-estuary movement. The study determined whether ebb-tide transport during the spawning migration is based upon an endogenous rhythm in vertical migration. Under constant conditions in a rectangular container, which limited horizontal and vertical movements, females with young and mature embryos had circatidal rhythms (periods=12.11-12.95 h) in migratory restlessness (swimming activity) and egg maintenance behavior (abdominal pumping). However, the rhythms were out of phase, as migratory restlessness occurred during the expected time of ebb tide in the field, and egg maintenance behavior, during the time of flood tide. Under constant conditions in vertical columns (1.32 m high), crabs with mature embryos had a circatidal rhythm (periods=12.2-13.7 h) in which they had frequent bouts of swimming to the surface of the column during the expected time of ebb tide in the field and remained on the bottom during the time of flood tide. This rhythm was not present in crabs with young embryos and disappeared after larval release. Thus, an endogenous rhythm in vertical migration does underlie the ebb-tide transport behavior of ovigerous blue crabs with mature embryos during their spawning migration.     

Photosynthesis and chlorophyll a fluorescence rhythms of marine phytoplankton

Circadian rhythms in photosynthesis were defined in field populations of phytoplankton. Measurements of carbon-dioxide fixation rates demonstrated that a diurnal periodicity of photosynthesis in samples incubated under natural light-dark (LD) cycles also were observed to continue in similar samples which had been photoadapted to constant dim light (LL) for 48 h. These changes in photosynthetic rates preceded sunset and sunrise, had daily amplitudes that ranged from 1.5 to 2.0, appeared to be independent of light-intensity, and displayed maxima about midday, while rates of dark fixation of carbon dioxide and the photosynthetic pigment content per cell were constant over the circadian cycle. Similar rhythmicity also was detected in room-temperature (22°C) chlorophyll a fluorescence yield, in both the obsence and presence of the photosynthesis inhibitor DCMU [3-(3,4-dichlorophenyl)-1, 1-dimethylurea]. However, the magnitude and timing of the fluorescence rhythm maxima seem to depend on wavelengths monitored and, in part, on the measuring technique used. Also, the circadian changes in the fluorescence intensity were abolished at low temperature (-60°C), and the shape of the emission spectra of chlorophyll fluorescence of cells in LD and LL did not change over time. The significance of the fluorescence rhythms with regard to chlorophyll a determinations and photosynthetic rates is discussed. It was concluded that there was sufficient similarity between circadian rhythms of photosynthesis in natural phytoplankton populations and in laboratory cultures of dinoflagellates to suggest that the mechanism of regulation may be the same for both of them.     

Effects of dusk and dawn on locomotor activity rhythms in the norway lobster Nephrops norvegicus

The endogenous locomotor activity rhythm of Nephrops norvegicus (L.) shows peaks during darkness, around 3 h after dusk. At the peaks, activity occurs mainly within the burrow, although the prawns repeatedly vacate the burrows during the same periods. The phase of the rhythm shifts with a change of light-dark regime and in response to changed timing of dusk when dawn is fixed. Activity is suppressed immediately at dawn, but recommences before complete darkness during gradually reduced light at simulated dusk. This difference in response to light at dusk and dawn indicates phase responsiveness which is characteristic of endogenous rhythms entrained by light. The light-entrained endogenous rhythm is complementary to the rhythm of emergence which, reflected in commercial catches, appears to be controlled by exogenous factors.