An entrainment model for semilunar rhythmic swimming behaviour in the marine isopod Eurydice pulchra Leach

Entrainment experiments have been carried out with geographically widely separated populations of the sand beach isopod Eurydice pulchra Leach subjected to periods of simulated tidal agitation imposed concurrently with a 24-h light: dark (L: D) cycle. Circatidal swimming rhythms of greatest amplitude were induced when agitation was applied with the subjective timing, within the L: D cycle, of local spring high tides. This occurred in a normal L: D regime and also when the L: D regime was phase shifted through 90°. Animals previously maintained in constant darkness (D: D) and subsequently exposed to simulated tidal disturbance at various times in constant darkness were unable to modulate the amplitude of circatidal swimming activity. Isopods previously maintained in a normal L: D cycle and subsequently subjected to artificial tidal agitation in constant darkness were, however, able to modulate circatidal activity. This indicates that E. pulchra is capable of detecting tidal agitation and daily light cues and using them in conjunction with its circadian “clock” to modulate its endogenous circatidal rhythmicity. The free-running semilunar rhythm of swimming activity entrained only when the timing of agitation within the day/night cycle mimicked the pattern of local spring high tides. Agitation with the timing of neap high tides entrained no free-running circa-semilunar activity pattern.     

A study of the endogenous activity rhythms of the marine isopod Exosphaeroma truncatitelson

The endogenous activity rhythms of the South African endemic isopod Exosphaeroma truncatitelson were explored. Isopods were collected on days coinciding with either a neap or spring tide. High- and low-energy beaches, which vary in the intensity of wave action, were selected as study sites. Isopods, in groups of 10–30, were placed in glass tanks with different experimental conditions: darkness + no sand, darkness with sand and natural ambient light (no sand). Activity of the isopods was measured for 50 h by recording the number of isopods swimming actively during a 30-s period. These isopods exhibited an endogenous activity rhythm which coincided with the tidal cycle even though removed from their natural habitat. Cosine curves were fitted to the observed activity data and statistical differences across variables were investigated. Peak activity was shown to occur shortly after high tide. Similar activity cycles were observed for both neap and spring tides and for different times of the year. Results also indicated that the activity cycles at both low- and high-energy beaches were similar. Two survival advantages of this rhythm are proposed: prevention of stranding on high shores and competitive avoidance with other local isopod species.     

Entrainment of the activity rhythm of the mole crab Emerita talpoida

The mole crab Emerita talpoida migrates with the tide in the swash zone of sand beaches. A circatidal rhythm in vertical swimming underlies movement, in which mature male crabs show peak swimming activity 1-2 h after the time of high tides at the collection site. In addition, there is a secondary rhythm in activity amplitude, in which crabs are maximally active following low amplitude high tides and minimally active following high amplitude high tides. The present study determined the phase response relationship for entrainment of the circatidal rhythm with mechanical agitation and whether the cycle in activity related to tidal amplitude could be entrained by a cycle in the duration of mechanical agitation at the times of consecutive high tides. After entrainment with mechanical agitation on an orbital shaker, activity of individual crabs was monitored in constant conditions with a video system and quantified as the number of ascents from the sand each 0.5 h. Mechanical agitation at the times of high tide, mid-ebb and low tide reset the timing of the circatidal rhythm according to the timing relationship to high tide. However, mechanical agitation during flood tide had no entrainment effect. In addition, a cycle in duration of mechanical agitation entrained the rhythm in activity amplitude associated with tidal amplitude. Both rhythms and entrainment effectiveness over the tidal cycle may function to reduce the likelihood of stranding above the swash zone.     

Rhythmic swimming behaviour of the New Zealand sand beach isopod Pseudaega punctata Thomson

The swimming rhythm of Pseudaega punctata Thomson is shown to have dual circadian and tidal components. The rhythm is endogenous, persisting for ten days under constant conditions in the laboratory and has a free-running period of greater than tidal frequency. The swimming activity has a basic semi-lunar rhythm even in the absence of marked differences between the heights of spring and neap tides. The rhythm is phased by exogenous factors such as light and tides but is flexible enough to deal with seasonal variations in day length and the shifting tidal cycle. Chilling weakly-rhythmic isopods re-inforces the rhythm. Control is thought to be neurosecretory, depletion of a neurosecretory product accumulated during a quiescent phase terminating swimming activity. The work is compared with similar studies on the related Eurydice pulchra which fills the same ecological niche in the northern hemisphere.     

Endogenous rhythms and entrainment cues of larval activity in the horseshoe crab Limulus polyphemus

The American horseshoe crab, Limulus polyphemus (Linnaeus), typically inhabits estuaries and coastal areas with pronounced semi-diurnal and diurnal tides that are used to synchronize the timing of spawning, larval hatching, and emergence. Horseshoe crabs spawn in the intertidal zone of sandy beaches and larval emergence occurs when the larvae exit the sediments and enter the plankton. However, L. polyphemus populations also occur in areas that lack significant tidal changes and associated synchronization cues. Endogenous activity rhythms that match predictable environmental cycles may enable larval horseshoe crabs to time swimming activity to prevent stranding on the beach. To determine if L. polyphemus larvae possess a circatidal rhythm in vertical swimming, larvae collected from beach nests and the plankton were placed under constant conditions and their activity monitored for 72 h. Time-series analyses of the activity records revealed a circatidal rhythm with a free-running period of ≈ 12.5 h. Maximum swimming activity consistently occurred during the time of expected falling tides, which may serve to reduce the chance of larvae being stranded on the beach and aid in seaward transport by ebb currents (i.e., ebb-tide transport). To determine if agitation serves as the entrainment cue, larvae were shaken on a 12.4 h cycle to simulate conditions during high tide in areas with semi-diurnal tides. When placed under constant conditions, larval swimming increased near the expected times of agitation. Thus, endogenous rhythms of swimming activity of L. polyphemus larvae in both tidal and nontidal systems may help synchronize swimming activity with periods of high water and inundation.     

Factors affecting the circatidal rhythm in vertical swimming of ovigerous blue crabs, Callinectes sapidus, involved in the spawning migration

Ovigerous blue crabs, Callinectes sapidus, are observed to undergo nocturnal ebb-tide transport (ETT) during their seaward spawning migration. A previous study found that females undergoing the spawning migration have a circatidal rhythm in vertical swimming, which serves as the biological basis for ETT. The present study asked three questions about this endogenous rhythm. First, does the rhythm occur in females with mature embryos regardless of whether they are undergoing ETT? Second, when exposed to a light/dark cycle in the laboratory, do ovigerous females only swim vertically at the time of ebb tide during the dark phase? Third, do attachments to the backs of ovigerous crabs affect the circatidal rhythm? The circatidal rhythm occurred in all crabs with mid-stage embryos that were prevented from undergoing ETT. The rhythm was unaffected by the light/dark cycle, which implies that migration can occur at lower light levels at depth during the day. Finally, attachments did not affect the rhythm, which suggests that tags and transmitters will not affect the spawning migration.     

Rhythms of Locomotion and Oxygen Consumption in the Estuarine Amphipod Corophium Volutator (Crustacea: Amphipoda)

The estuarine amphipod Corophium volutator exhibits an endogenous circatidal rhythm of swimming activity, with maxima occurring just after the expected time of high water, under constant laboratory conditions. Oxygen uptake by Corophium is also subject to modulation across the tidal cycle. The period of highest oxygen uptake occurs during the ebb tide, in phase with the period of maximum swimming activity. A second increase in oxygen uptake during the early flood tide is thought to reflect either in-burrow activity or a previously described rhythm of emergence. This being so, this aspect of the animal's respiratory metabolism may be regulated by an autonomous oscillator independent of that governing the animal's swimming behaviour.     

Activity and feeding of Dotilla fenestrata (Brachyura: Ocypodidae) in a warm,temperate South African estuary

The activity of and consumption of organic material by the sand-bubbler crab Dotilla fenestrata was studied over neap and spring tides on a sheltered sand bank close to the mouth of the warm, temperate Kowie Estuary, South Africa. Crabs emerged from their burrows only after the tide receded, and it was light. Time to emergence therefore varied from about 30 minutes to three hours after exposure, depending on the time of low water in the early morning vs at midday. General activity of the crab population was longer on a spring tide (about five hours) than on a neap tide (about three hours). Maximum densities of active crabs were 140 m^–2 and 41 m^–2 on spring and neap tides, respectively. After emergence, crabs spent 60% to 80% of their time feeding. In the Kowie Estuary, D. fenestrata produced between 7 and 12 pseudofaecal pellets, average weight 0.0358 g per pellet, per minute. These pellets had a significantly lower organic and chlorophyll a content than the substratum, and it was estimated that crabs removed about 25% of the organic content from the sediment.     

Developmental shift in the selective tidal-stream transport behavior of larvae of the fiddler crab Uca minax (LeConte)

Following hatching, larvae of the fiddler crab Uca minax (La Conte) are exported from the adult habitat in estuaries to coastal and shelf waters where they undergo development prior to re-entering estuaries as postlarvae (megalopae). Studies of the spatial distribution of both newly hatched zoeae (Stage I) and megalopae indicate they undergo rhythmic vertical migrations associated with the tides for dispersal and unidirectional transport (selective tidal-stream transport) both within estuaries and between estuaries and the nearshore coastal ocean. We tested the hypothesis that U. minax zoeae possess a circatidal rhythm in vertical migration that facilitates offshore transport in ebb tidal flows, while postlarvae (megalopae) return to estuaries using a similar flood-phased endogenous rhythm. We also determined if the expression of the rhythm was influenced by the salinity conditions zoeae and megalopae experience as they transition between low-salinity regions of estuaries and high-salinity coastal waters. Stage I zoeae were collected by holding ovigerous female crabs in the lab until hatching. Megalopae were collected from the plankton and identified to species using molecular techniques (PCR-RFLP). Under constant laboratory conditions, both zoeae and megalopae exhibited endogenous circatidal rhythms in swimming that matched the principal harmonic constituent of the local tides (12.39 ± 0.07 h; X¯ ± SE). Upward swimming in Stage I zoeae occurred 2.5-4 h after high tide near the time of expected maximum ebb currents in the field. Rhythmic swimming of megalopae occurred slightly earlier in the tide (2.5 ± 0.09 h after high tide; X¯ ± SE) but was not entirely synchronized with flood currents, as expected. Salinity conditions had no apparent effect on the expression or pattern of the rhythms. Results indicate that this circatidal rhythm forms the behavioral basis of selective tidal-stream transport (STST) in early stage U. minax zoeae, but does not undergo a sufficient phase shift to account for vertical distribution patterns exhibited by megalopae in the field.     

Clock control of foraging in the isopod Scyphax ornatus Dana

Abstract

The terrestrial sand beach isopod Scyphax ornatus Dana exhibits circadian and circa-semilunar activity rhythms when kept in constant conditions in the laboratory. The circadian rhythm restricts activity to the subjective night and can be synchronised to artificial light cycles. The circa-semilunar rhythm is expressed as a cyclic variation in overall activity level, with isopods alternately active on 6–8 consecutive nights and then inactive on the next 6–8 nights. The circa-semilunar rhythm matches a fortnightly cycle in food availability on the isopods’ home beach, but does not appear to be causally related to the lunar cycle, the spring/neap tidal cycle, or to moulting. This and other evidence suggests that the ecologicalrole of the endogenous circa-semilunar rhythm is to allow Scyphax, within the protection of their burrows, to predict nightly foraging opportunities; a new role for such a long-period rhythm.     

Time-keeping system of the eel pout, Zoarces viviparus

Observations on the rhythmic activity of 71 juvenile specimens of the inter-tidal blenny Zoarces viviparus reveal an endogenous pattern of swimming at three different periodicities. Circatidal swimming, with activity peaks phased to high water or the ebb of the subjective 12.4-h tides, was found in 50 fish and was the predominant pattern seen immediately after collection, when the rhythm generally persisted for between 3 and 12 cycles. Discrete activity peaks, with a free running period of approximately 24 h were also evident in the swimming pattern of eight fish. A circadian influence was also manifest as a modulation in amplitude, phase shifts and changes in free-running period of the circa-tidal rhythm. Overall, the activity level declined with time but those fish that remained active long enough showed a semi-lunar rhythm, with maximum activity at the time of the spring tides. A comparison of the behavior of animals collected at different times of the year suggests a seasonal variation in the persistence of circatidal swimming. The results are consistent with a control system involving circatidal, circadian, and semi-lunar oscillators. (Chronobiology International, 18(1), 27-46, 2001)     

TIME-KEEPING SYSTEM OF THE EEL POUT,ZOARCES VIVIPARUS

Observations on the rhythmic activity of 71 juvenile specimens of the inter-tidal blenny Zoarces viviparus reveal an endogenous pattern of swimming at three different periodicities. Circatidal swimming, with activity peaks phased to high water or the ebb of the subjective 12.4-h tides, was found in 50 fish and was the predominant pattern seen immediately after collection, when the rhythm generally persisted for between 3 and 12 cycles. Discrete activity peaks, with a free running period of approximately 24 h were also evident in the swimming pattern of eight fish. A circadian influence was also manifest as a modulation in amplitude, phase shifts and changes in free-running period of the circa-tidal rhythm. Overall, the activity level declined with time but those fish that remained active long enough showed a semi-lunar rhythm, with maximum activity at the time of the spring tides. A comparison of the behavior of animals collected at different times of the year suggests a seasonal variation in the persistence of circatidal swimming. The results are consistent with a control system involving circatidal, circadian, and semi-lunar oscillators. (Chronobiology International, 18(1), 27–46, 2001)     

Environmental entrainment of tidally rhythmic behaviour in marine animals

Field and laboratory experiments show that endogenous circatidal rhythms in coastal animals are entrained by exposure to real or simulated tidal cycles of hydrostatic pressure, temperature, salinity, wave agitation, immersion and light. Short pulses (2–3 h) of simulated high tide induce slight phase advances or delays in the free-running circatidal rhythm of groups of experimental animals, depending upon the time of application. Phase-response curves derived in this way are less clear-cut than for typical circadian rhythms, but their pattern suggests that tidally rhythmic behaviour is controlled by truly circatidal (and not circadian) oscillators. The underlying circatidal oscillators appear, in general, to be fairly stable, suggesting that populations of coastal animals are relatively unsusceptible to irregularly timed environmental stimuli associated, say, with severe storms.     

Circadian and circatidal rhythms of oxygen consumption in the sandy-beach isopod Tylos granulatus Krauss

The sandy-beach isopod Tylos granulatus Krauss burrows at the high tide mark, and has rhythms of nocturnal emergence coincident with the low tide period. Measurements of the respiration rate show that a low rate of oxygen consumption is maintained throughout the day but there is a circatidal rhythmic increase of between 300 and 700% during the nocturnal low tide. The height of this peak and the percentage of animals displaying a peak both increase from spring tide to neap tide suggesting a semi-lunar rhythm. The respiratory peaks have a 24.8 h periodicity, being later each night until low tide falls in the dawn, when there is a ‘switch-back’ so that peaks are then during the subsequent evening low tide. These respiratory rhythms are persistent under constant light and coincide with previously described activity rhythms. The respiratory rhythms considerably reduce metabolic energy losses, particularly as the activity rhythms ensure avoidance of high diurnal temperatures and activity during the cooler nocturnal period.     

Ontogeny of an endogenous rhythm in Eurydice pulchra

Field catches of Eurydice pulchra (Leach) from an Isle of Man beach indicated that adult animals were active in the water column solely during spring tide periods, whereas juvenile animals swam abundantly at high tide irrespective of lunar phase. Under constant conditions in the laboratory, animals kept in actographs with sand showed a circa-tidal rhythm of spontaneous emergence and swimming activity. In adults, the activity was greatest during “expected” night-time high-waters and was expressed solely after collection during spring tide periods. The rhythm was independent of sex, season or reproductive status. Juveniles showed no such diurnal modulation of the rhythm and the pattern was expressed throughout the semi-lunar cycle. These ontogenetic differences in behaviour are discussed in the light of previous work on the rhythm, and in terms of the differing habits of the mature and immature animals.     

Circatidal rhythmic behaviour in the coastal tiger beetle Callytron inspecularis in Japan

Larvae of the coastal tiger beetle Callytron inspecularis (W. Horn) (Coleoptera: Cicindelidae) plug their burrow opening before submergence at high tide. Field observations showed that burrow plugging was a rhythmic behaviour that coincided with the tidal cycle (ca. 12.4 h). On average, larvae plugged their burrows 41.8 min before the tide covered the habitat. The mean interval between consecutive burrow-plugging events in the field was 12.40 h. In the laboratory, in the absence of tidal inundation, the mean interval between consecutive burrow-plugging events was 12.45 h. This suggests that the burrow-plugging rhythm of the coastal tiger beetle is governed by an endogenous circatidal rhythm.     

Field measurements and modeling of groundwater flow and biogeochemistry at Moses Hammock, a backbarrier island on the Georgia coast

A combination of field measurements, laboratory experiments and model simulations were used to characterize the groundwater biogeochemical dynamics along a shallow monitoring well transect on a coastal hammock. A switch in the redox status of the dissolved inorganic nitrogen (DIN) pool in the well at the upland/saltmarsh interface occurred over the spring-neap tidal transition: the DIN pool was dominated by nitrate during spring tide and by ammonium during neap tide. A density-dependent reaction-transport model was used to investigate the relative importance of individual processes to the observed N redox-switch. The observed N redox-switch was evaluated with regard to the roles of nitrification, denitrification, dissimilatory nitrate reduction to ammonium (DNRA), ammonium adsorption, and variations in inflowing water geochemistry between spring and neap tides. Transport was driven by measured pressure heads and process parameterizations were derived from field observations, targeted laboratory experiments, and the literature. Modeling results suggest that the variation in inflow water chemistry was the dominant driver of DIN dynamics and highlight the importance of spring-neap tide variations in the high marsh, which influences groundwater biogeochemistry at the marsh-upland transition.     

A comparison of the activity patterns of the sand goby Pomatoschistus minutus (Pallas) from areas of different tidal range

Sand gobies ( Pomatoschistus minutus ) collected from beaches with a large tidal range (Scotland) exhibit a circatidal rhythm of activity in constant conditions in the laboratory. There is no endogenous circadian component to the rhythm. The phasing of the rhythm is such that peak activity occurs at the predicted time of ebb tide. Light-dark (LD) cycles applied in the laboratory have a marked effect on activity greatly enhancing it at night so that the original tidal rhythm becomes nocturnal. Some evidence was obtained that LD cycles can entrain a weak nocturnal circadian rhythm in fish removed from tidal conditions. Contrary to expectations, some fish from beaches with a small and unpredictable tidal range (Oslofjord, Norway) also show a weakly persistent circatidal thythm without an endogenous circadian component, but great variability was noticed between individual fish. Laboratory LD cycles did not entrain a persistent circadian rhythm in the fish from the Oslofjord.     

Linkages between seagrass,mangrove and saltmarsh as fish habitat in the Botany Bay estuary,New South Wales

Shallow-water vegetated estuarine habitats, notably seagrass, mangrove and saltmarsh, are known to be important habitats for many species of small or juvenile fish in temperate Australia. However, the movement of fish between these habitats is poorly understood, and yet critical to the management of the estuarine fisheries resource. We installed a series of buoyant pop nets in adjacent stands of seagrass, mangrove and saltmarsh in order to determine how relative abundance of fishes varied through lunar cycles. Nets were released in all habitats at the peak of the monthly spring tide for 12 months, and in the seagrass habitat at the peak of the neap tide also. The assemblage of fish in each habitat differed during the spring tides. The seagrass assemblage differed between spring and neap tide, with the neap tide assemblage showing greater abundances of fish, particularly those species which visited the adjacent habitats when inundated during spring tides. The result supports the hypothesis that fish move from the seagrass to the adjacent mangrove and saltmarsh during spring tides, taking advantage of high abundances of zooplankton, and use seagrass as a refuge during lower tides. The restoration and preservation of mangrove and saltmarsh utility as fish habitat may in some situations be linked to the proximity of available seagrass.     

Foraging strategy of the mudskipper Periophthalmus sobrinus Eggert in a Kenyan mangrove

The feeding behaviour of Periophthalmus sobrinus was studied in a population living along the channels of the Tana river delta. In November 1993 mudskippers were sampled every 2 tidal h for two consecutive spring and neap tides both during the day and night. The fishes were sexed and their stomach contents analysed. The results indicated that the mudskipper has a carnivorous diet and forages during both day and night although feeding greatly decreases after dark. Quantitative and qualitative differences in diet were found during the day and night of the two synodic and tidal phases. These differences were also demonstrable in the two sexes. The study showed that females of P. sobrinus are more selective than males and that differences between the two sexes may be related to reproductive condition. Furthermore, the mudskippers showed a tidal rhythm in feeding behaviour with peaks of activity around low tide (LT) on spring tides and around high tide (HT) on neap tides. Foraging activity seems to be influenced by the different spatial and temporal distributions of the mudskipper's prey caused by synodic, tidal and diel changes in the environment.