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.     

Persistent bimodal activity patterns in wild and captive black-tailed godwit <Emphasis Type="Italic">Limosa limosa</Emphasis> under different environmental conditions

There is a large literature dealing with daily foraging routines of wild birds during the non-breeding season. While different laboratory studies have showed that some bird activity patterns are a persistent property of the circadian system, most of field studies preclude the potential role of an endogenous circadian rhythm in controlling bird’s foraging routines. In this study we compared the patterns of diurnal foraging activity and intake rates of migrating black-tailed godwits, Limosa limosa (radio-tagged and non-tagged individuals) at two stopover sites (habitats) with different environmental characteristics, aiming at identifying proximate factors of bird activity routines. To gain insights into the role of food availability in control of such foraging routines, we also estimated foraging activity patterns in captive godwits subjected to constant food availability. Captive and wild black-tailed godwits showed a persistent bimodal activity pattern through daylight period. Food availability had a significant effect on the intake rates, but had a subtler effect on foraging and intake rate rhythms. Temperature and wind speed (combined in a weather index) showed non-significant effects on both rhythms. Although we could not discard a role for natural diurnal changes in light intensity, an important timing cue, our findings support the idea that an endogenous circadian rhythm could be an important proximate factor regulating foraging activity and food items taken per unit time of wild black-tailed godwits during migration.     

The role of the queen in circadian rhythms of honeybees (Apis mellifera L.)

Summary Colonies and smaller social groups of honeybees (Apis mellifera carnica L.) show distinct free-running circadian rhythms similar to that of individual organisms. The workers of a colony synchronize their individual rhythms to one overall group rhythm. Caste plays an important role in this synchronization process. Queens were introduced into worker groups which were entrained to a phase-shifted light/dark cycle. The introduction of the queen caused a shift in the free-running phase under constant dark conditions. Single introduced workers had no effect on the free-running rhythms. This indicates that the queen plays an important role in the synchronization of circadian rhythms of honeybee colonies.     

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.     

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.     

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.     

Circannual variations of lizard circadian activity rhythms in constant darkness

The daily pattern of locomotor activity of Podarcis sicula in the field changes from unimodal in spring to bimodal in summer, becoming unimodal again in autumn. Short-term experiments in which P. sicula collected in different months were tested under constant conditions immediately after capture showed that the activity pattern typical of each season is retained in the lizard circadian locomotor rhythm. In constant conditions, the bimodal pattern is associated with a short free-running period (τ) of the circadian locomotor rhythm and a long circadian activity (α), while the unimodal pattern is associated with a long τ and short α. To test whether seasonal changes in circadian locomotor rhythms are driven by a circannual clock, we recorded locomotor activity of lizards over 12–15 months in constant temperature and darkness. The present results demonstrate, for the first time in a vertebrate, the existence of circannual changes in constant darkness of both τ and α. In most lizards, the longest τ along its circannual cycle is associated with a short α, and the shortest τ in the same cycle with a long α, so that the pattern of mutual association between τ and α is the same as in short-term experiments. Most lizards, however, stayed unimodal all the time. This shows that changes in activity pattern from unimodal to bimodal (and vice versa) are induced by seasonal changes in environmental factors, instead of being incorporated into a circannual rhythm. Circannual changes in τ and α of locomotor rhythms may adaptively predispose the circadian system of P. sicula to a change in activity pattern as soon as seasonal changes in the environment demand it. Received: 22 January 1999 / Received in revised form: 14 April 1999 / Accepted: 19 April 1999     

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.     

Hatching rhythms in Uca pugilator (Decapoda:Brachyura)

Gravid female Uca pugilator (Bosc) maintained in conditions of 14h L: 10h D light regime and constant temperature without simulated tides showed a significant positive correlation between time of hatch and time of the nighttime high tide. Light: Dark experiments showed no entrainment by LD cues. Larval hatching was delayed until dark when high tide occurred between 1900 and 2130 hrs. Hatch time was a positive linear function of the time of the nighttime high tide when high tide occurred after 2130 hrs. Time of hatch was delayed by the light period on days lacking a nighttime high tide. Experiments conducted under constant light (LL) and temperature, without simulated tides, indicated a persistent free-running rhythm of approximately 25 h 03 min, suggesting an endogenous timer. Rhythmic larval release on the nighttime high tide may be adaptive as a predator-avoidance mechanism for adult gravid females.Contribution No. 366 from the Belle W. Baruch Institute for Marine Biology and Coastal Research, University of South Carolina     

Self-organization of circadian rhythms in groups of honeybees (Apis mellifera L.)

Workers in social groups of honeybees (Apis mellifera L.) synchronize their individual free-running circadian rhythms to an overall group rhythm. By monitoring the activity of bees by recording the oxygen consumption and intragroup temperature, it is shown that the rhythm coordination is in part achieved by temperature fluctuations as an intragroup Zeitgeber. Trophallaxis was shown to have only a minor (if any) effect on circadian rhythm synchronization. A model incorporating a feed back loop between temperature and activity can plausibly explain the observed synchronization of individual rhythms in social groups as a self-organization phenomenon. Correspondence to: R.F.A. Moritz     

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     

Ontogenetic differences in the circadian locomotor activity rhythm of the talitrid amphipod crustacean Orchestoidea tuberculata

 Adult talitrid amphipods often display a nocturnal activity pattern, which has been shown in a number of cases to be partly controlled by an endogenous rhythm of circadian period. Juvenile talitrids have been little studied in the past, but evidence from field studies indicates that they may display a different diel pattern of locomotor activity from that of adults. This study presents evidence from the field in south–central Chile that juvenile Orchestoidea tuberculata Nicolet show crepuscular activity peaks, contrasting with the nocturnal peaks shown by adult conspecifics. Under constant conditions in the laboratory, both juveniles and adults exhibit endogenous rhythms of circadian periodicity. However, the phasing of activity differs in juveniles and adults, corresponding to the differences observed in the field. It is suggested that differing phasing of peak locomotor activity may be a mechanism to reduce contact between juvenile and adult talitrids. Experimental evidence indicates a significant negative influence on survival of juveniles in the presence of adult conspecifics by intraspecific predation. Other factors influencing the timing of surface activity are also discussed. Received: 3 August 1999 / Accepted: 26 May 2000     

Lack of social entrainment of free-running circadian activity rhythms in the Australian sugar glider (Petaurus breviceps: Marsupialia)

Summary Social influence on circadian activity rhythms was investigated in the nocturnal Australian marsupial Petaurus breviceps. The activity of two and two was recorded electroacoustically and observed by an IR television camera in LD 12:12 (10¹:10^-1lx) and in LL (10^-1lx) when housed isolated and in pairs (+). In LD-entrained animals the average duration of locomotion, orientation movements, grooming and total activity is influenced by social housing, and individually different activity patterns are harmonized. In constant illumination conditions, however, the members of a pair are not mutually synchronized and free-run with different circadian periodlengths. Therefore social influence on the LD-entrained activity rhythm in Petaurus should be interpreted as social masking rather than direct influence on the circadian system.     

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     

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.     

Circadian rhythms in the respiration of eight species of cardinal fishes (Pisces: Apogonidae): comparative analysis and adaptive significance

A comparative study was made of the entrained (12:12 LD) and endogenous (DD) respiratory rhythms of 8 species of cardinal fishes. Volumetric respirometers, designed specifically for long-term measurements of oxygen uptake by small fishes under controlled conditions, were used during standard 5 day experiments. Despite some individual variation, certain species-specific and genus-specific patterns of respiration emerged. Each species showed a persistant (advancing) rhythm of oxygen consumption during 3 days of DD. Light appeared to be the Zeitgeber, with the light-dark transition phasing the nocturnal peaks and the dark-light transition possibly phasing the diurnal ones. Genus-specific and species-specific trends in field behavior, habitat selection, and distribution were studied. There were correlations between the field behavior and the entrained respiratory rhythms of these nocturnally active fishes. Entrained and endogenous rhythms of each species showed characteristic similarities and were interpreted as integral components of a level of organization evolved for nocturnal life in the shallow marine environment.     

Kinetics of light-intensity adaptation in a marine planktonic diatom

The marine planktonic diatom Thalassiosira weisflogii was grown in turbidostat culture under both continuous and 12 hL: 12 hD illumination regimes in order to study the kinetics of adaptation to growth-irradiance levels. In both illumination regimes adaptation to a higher growth-irradiance level was accompanied by an increase in cell division rates and a decrease in chlorophyll a cell^-1. The rates of adaptation for both processes, derived from first order kinetic analysis, equaled each other in each experiment. The results suggest that during the transition from low-to-high growth-irradiance levels chlorophyll a is diluted by cell division and is not actively degraded. Introduction of a light/dark cycle lowered the rate of adaptation. In transitions from high-to-low growth-irradiance levels there was a sharp drop in growth rates and a slow increase in chlorophyll a cell^-1 under both continuous and intermittent illumination. In the 12 hL:12hD cycle there was a circadian rhythm in chlorophyll a cell^-1, where cellular chlorophyll contents increased during the light cycle and decreased during the dark cycle. This circadian rhythm was distinctly different from light intensity adaptation. For kinetic analysis of light intensity adaptation in a 12 hL: 12 hD cycle, the circadian periodicity was separated from the light intensity response by subjecting the data to a Kaiser window optimization digital filter. Kinetic parameters for light-intensity adaptation were resolved from the filtered data. The kinetics of lightintensity adaptation of marine phytoplankton are discussed in relation to their spatial variations and time scales of mixing.This research was performed at Brookhaven National Laboratory under the auspices of the United States Department of Energy under Contract No. DE-AC02-76 CH00016     

Social synchronization of circadian rhythms in deer mice (Peromyscus maniculatus)

Summary Deer mice (Peromyscus maniculatus), kept in individual cages under constant dim-light conditions, displayed steady free-running rhythms of activity, the period of which varied between individuals.When two previously isolated mice with different rhythms were placed in a common enclosure, under the same constant light conditions, they soon displayed a mutual synchronization of their activity rhythms. When separated again, the mice lost mutual synchronization (Figs. 1 and 2)The process by which mutual synchronization was attained in the common enclosure is typical of entrainment by an external synchronizer (Zeitgeber). Our results suggest that the activity rhythm of the dominant mouse entrains the activity rhythm of the subordinate, and is thus a social Zeitgeber.     

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.