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     

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.     

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 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.     

Environmental influence on the locomotor activity rhythm of Talitrus saltator (Crustacea: Amphipoda)

The persistence and precision of the endogenous, nocturnal, circadian locomotor rhythm of the sand-beach amphipod Talitrus saltator is characterised, and the influence of substrate availability, photoperiod, temperature and relative humidity as potential environmental synchronizers of the rhythm is assessed. Individual, cyclic light-dark and temperature regimes synchronize and modify the laboratory activity pattern, but substrate availability and relative humidity have no significant long-term effect. Under simulateneous experimental regimes simulating field conditions of photoperiod, temperature and relative humidity the rhythm is entrained solely by photoperiod. The implications are discussed in relation to field behaviour.     

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.     

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.     

Endogenous swimming rhythms of blue crab, Callinectes sapidus , megalopae: effects of offshore and estuarine cues

Larvae of the blue crab Callinectes sapidus Rathbun develop on the continental shelf. The postlarval stage (megalopa) occurs near the surface and is transported shoreward by wind-driven surface currents. It then uses selective tidal stream transport for migration up an estuary. Endogenous swimming rhythms were measured under constant dark conditions in the laboratory in megalopae collected from the Newport River Estuary (North Carolina), the Delaware Bay, and offshore from the Newport River Estuary. Megalopae from all areas had a similar circadian activity rhythm, in which they swam during the time of the day phase in the field and were inactive at night. This rhythm predicts the presence of a reverse, diel, vertical-migration pattern offshore which would contribute to the location of megalopae near the surface during the day. The rhythm lacks obvious ecological significance in estuaries because it does not contribute to selective tidal stream transport and would increase vulnerability to visual predators during the day. Attempts to entrain a circatidal rhythm in swimming by cyclic and step changes in salinity were unsuccessful, as the circadian rhythm persisted. The rhythm also continued in the presence of the eelgrass Zostera marina, which is a site of settlement and metamorphosis in the field. Thus, megalopae enter estuaries with a solar day rhythm in activity. This rhythm, however, is not expressed, because light inhibits swimming during the day upon exposure to estuarine water. Since this light inhibition is removed in offshore waters, the rhythm would be expressed if, after entering an estuary, megalopae were transported back to offshore areas. Received: 19 December 1995 / Accepted: 2 August 1996     

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.     

Temporal patterns of shell-gape in Mytilus edulis

Hitherto published evidence of the presence or absence of endogenous activity rhythms in bivalve molluscs is equivocal. Mytilus edulis L. were collected from a North Wales (UK) estuary in 1985, and shell-gaping was investigated in individual mussels under constant conditions in the laboratory. Results suggest that there is no endogenous circatidal rhythm of shell-gaping in this species, This is consistent with the view that, unlike mobile species, sessile intertidal species are much more likely to exhibit exogenous rather than endogenous responses to tidal fluctuations. There is some evidence of weak circadian rhythmicity of shell-gaping in M. edulis, with greater duration of shell-closure during hours of expected daylight. Such behaviour could represent an adaptational defence against visually-feeding predators.     

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.     

Light and social effects on the free-running circadian activity rhythm in common marmosets (Callithrix jacchus; Primates): social masking,pseudo-splitting,and relative coordination

Summary The variability of period of the free-running circadian activity rhythm (CAR) and the degree to which it is affected by social factors was studied in diurnal marmosets (Callithrix jacchus: Primates, Cebidae), kept either singly or in pairs. Under continuous light intensities between 10^-1 and 10² lx, the spontaneous period was always shorter than 24h. It varied in relation to the amount of time spent under constant conditions (after-effects). There was some evidence of an effect of light intensity on free-running period, but no clear correlation between the two. Mutual acoustic social contact caused some males to exhibit pseudo-splitting, ascribable to positive social masking, and in many cases also resulted in relative coordination of the free-running CAR. True social entrainment, however, was not produced. The possibility that the latter could occur under some conditions is discussed, as well as the neural pathways that might mediate the observed acoustically induced social effects on the central nervous system pacemaker(s) of the circadian timing system.     

Rhythmic motor activity responses of the California fiddler crab Uca crenulata to artificial light conditions

Uca crenulata, the California species of fiddler crab, was exposed to artificial light conditions to separate the influence of the light cycle from that of the tidal input on its rhythmic motor activity. Under both constant light and light-dark cycles, rhythmic activity was demonstrated in only 50% of the experimental crabs; the activity of the remaining 50% was random. Individuals exposed to constant light conditions after having been subjected to 24 h light-dark cycles demonstrated no significant difference in period length of their rhythmic activity from crabs investigated in constant light immediately after field collection. The mean period did not differ significantly from the tidal period of 24.8 h, but the variation was considerable. In artificial light-dark cycles, the activity rhythms were usually masked but, in some cases, synchronized. The results indicate that U. crenulata has an endogenous rhythm with a period close to the tidal cycle which may be synchronized by light as well as by tidal cues. The display of this endogenous rhythm, however, is poor.     

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.     

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.     

Vertical migratory rhythms of benthic diatoms in a tropical intertidal sand flat: influence of irradiance and tides

Vertical migratory behavior of benthic diatoms is one of the adaptive strategies employed for a life in intertidal habitats. Irradiance and tides are considered to be the key factors governing vertical migration. Experiments were carried out to determine the influence of these factors in a tropical intertidal sand flat. Rising to the sediment surface for fulfilment of their light requirements for photosynthesis was the first priority. If not fulfilled during the low-tide exposure, diatoms could withstand the tidal effects and stay up at the surface even during the high-tide coverage. In the laboratory experiments, where the effects of tides were removed, the endogenous clock continued to operate in a similar fashion to that in the field when under 12-h light:12-h dark conditions, whereas continuous darkness induced a tidal rhythm. In continuous light, diatoms preferred to stay up longer than was observed in field. The above-mentioned observations reveal that irradiance has a stronger effect than tides in controlling/regulating microscale migrations in benthic diatoms. In addition, temporal differences in the irradiance and the resulting changes in diatom migration can have implications for littoral primary productivity.Communicated by O. Kinne, Oldendorf/Luhe     

Relationships between intertidal zonation and circatidal rhythmicity in littoral gastropods

The presence and phase of circatidal rhythmicity was correlated with vertical zonation and other ecological factors. Ten species were studied in the field and in aktographs under controlled conditions in the laboratory. Retina plicata, Melanerita atramentosa, Bembicium nanum, Austrocochlea obtusa and Morula marginalba occupied mid- or upper-littoral zonations, and were subjected to regular tidal influence. They were active at high water and for a period after the ebb, possibly as these were the times of least desiccation. Each possessed a circatidal activity rhythm under non-tidal conditions. Midlittoral Amphinerita polita and lower-littoral Theliostyla albicilla were active at low water, possibly because their prefered habitats reduced desiccation and other selective forces, for example wave action and predation, determined the phase of the rhythmicity. Supra- and upper-littoral Nodilittorina pyramidalis and Melarapha unifasciata and lower- and infralittoral specimens of Bembicium auratum displayed no overt circatidal rhythmicity, possibly because they were not subjected to regular tidal action.     

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     

Relationship of daily and circatidal activity rhythms of the fiddler crab,<Emphasis Type="Italic"> Uca princeps</Emphasis>, to the harmonic structure of semidiurnal and mixed tides

Intertidal organisms may employ circatidal rhythms to track the tidal cycle, but tidal patterns may vary within a species range and necessitate adaptation to the local tides. Circatidal rhythms were examined in populations of the eastern Pacific fiddler crab Uca princeps (Smith) from four sites with differing tidal characteristics, La Paz (24°10N; 110°21W), San Blas (21°33N; 105°18W) and Manzanillo (19°6N; 104°24W), Mexico (lower amplitude, mixed semidiurnal tides) and Mata de Limon, Costa Rica (9°55N; 84°43W) (high-amplitude, semidiurnal tides). Local tides were characterized by harmonic constants of M₂, S₂, K₁, and O₁, partial tides that largely determine their semidiurnal and diurnal features. Rhythmic structure in continuously recorded locomotor activity of individual crabs held under laboratory conditions was described by cosinor and periodogram methods of time-series analysis. Both daily and circatidal rhythms were found in crabs studied in light–dark cycles set to local conditions at the time of collection. Crabs at all four sites shared a tendency toward bimodality, with a mid-morning activity peak and varying degrees of nocturnal activity. Circatidal rhythms closely matching the period of the 12.42-h M₂ partial tide were consistently present at all sites except Manzanillo. At Mata de Limon, the circatidal rhythm clearly dominated locomotor activity, but was strongly modulated by a daily rhythm in a repeating pattern at a semilunar interval. In contrast, the amplitude of the daily rhythm was higher than that of the circatidal rhythm in crabs from the three mixed tide sites on the Mexican coast, where the tidal pattern is dominated by a diurnal inequality arising from the diurnal K₁ and O₁ partial tides. These results suggest that populations of U. princeps use both daily and circatidal timing systems to track local forms of the tide generated by their M₂, S₂, K₁, and O₁ geophysical counterparts.Communicated by J.P. Grassle, New Brunswick