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.     

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.     

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.     

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     

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.     

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.     

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.     

Activity of root voles (Microtus oeconomus) under snow: social encounters synchronize individual activity rhythms

Microtine rodents usually display short-term activity rhythms synchronized by light. Social interactions have also been suggested to act as a zeitgeber, entraining individual activity, but evidence supporting this is scarce. In areas with a permanent snow cover during winter, small rodents spend most of the time in the subnivean space, between the snow cover and the ground, where they most likely are unaffected by otherwise dominating photoperiodic cues. The subnivean space, however, is fragmented, and this limits movement and may isolate individuals living just a few meters apart. These conditions provide excellent opportunities to test for the existence of social synchronization. During two winters, I experimentally decreased the subnivean fragmentation by placing out a network of corrugated aluminium sheets on the ground before snowfall, thus increasing the potential for movement and social interaction within the subnivean space. Other areas were left as controls. Intensive PIT-tag monitoring in the subnivean system provided individual activity data of root voles (Microtus oeconomus) without disturbing normal activity. The data revealed that microtines under snow displayed a free-running activity rhythm and that the activity was evenly distributed throughout the 24-h day, indicating a lack of photo-entrainment. Despite this lack of light, interacting individuals were synchronous, and pairwise synchrony decreased with decreasing potential for social interactions. These results suggest that social interactions indeed entrain microtine activity. Several possible adaptive advantages of the synchrony of microtine rodent activity have been proposed, and these theories are discussed in light of the result presented.     

Diurnal and circadian rhythms in the turbidity of growing Skeletonema costatum cultures

Skeletonema costatum (Grev.) Cleve grown in batch culture at low light intensity under a 14 h light: 10 h dark photocycle showed exponential cell proliferation (1.1 doublings d^-1) without significant phasing of the cell division by the light: dark cycle. The growth in carbon concentration was, however, restricted to the light period. The turbidity of the culture closely followed the carbon oattern, and was not affected by the increase in the cell number during the dark period. It was found that a trustule suspension had only approximately 1% of the turbidity of the corresponding intact algae. Culture turbidity was therefore regarded as a biomass parameter similar to the carbon concentration, without direct correlation to the timing of the cell division. The short-time variations in the turbidity of growing algal cultures were further studied in a cage culture turbidostat. The growth rate (based on turbidity) increased rapidly during the first half of the light period, decreased slightly towards the evening and was zero throughout the dark period. When transformed to continuous light, the growth of the culture continued to show damped oscillations for up to 1 wk, but with a period of 26.7 h instead of 24 h. The same circadian rhythm was observed in chlorophyll content, and is thus possibly a reflection of a freely oscillating internal biological clock. The cage culture turbidostat was found to be a suitable device for studies of the photocycle related regulation of biosynthesis in S. costatum.     

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     

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     

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     

Silver nanoparticles toxicity effect on photosystem II photochemistry of the green alga Chlamydomonas reinhardtii treated in light and dark conditions

The inhibitory effect of silver nanoparticles (AgNPs) on photochemical reactions of photosynthesis was investigated using the green alga model Chlamydomonas reinhardtii. Algal cells were exposed to 1, 5, and 10?µmol?L^?1 of AgNPs under both light and dark conditions during 6?h. The rapid rise of chlorophyll a fluorescence and the fluorescence imaging system were employed to investigate the alteration of photosystem II (PSII) photochemical reactions and the associated electron transport activity. When algal cells were exposed to 5 and 10?µmol?L^?1 of AgNPs, our results showed the evidence of a structural deterioration of PSII reaction center, the alteration of the oxygen evolving complex and the inhibition of electron transport activity, which was stronger for AgNPs treatment under light exposure. Under these conditions, there was no activation of regulated photoprotective mechanisms against excess absorbed light-energy by the antenna system of the PSII complex. The highest deteriorating effect on the structural and functional integrity of PSII was observed for algal cells exposed 6?h in light condition to 10?µmol?L^?1 of AgNPs. Therefore, we provide valuable data in this study permitting to use photosynthetic-based fluorescence parameters for aquatic toxicological risk investigation of polluted water that may contain AgNP suspension.     

Daily rhythm of O2-evolution in the cyanobacterium Trichodesmium thiebautii under natural and constant conditions

The rate of oxygen evolution by the tropical marine cyanobacterium Trichodesmium thiebautii was recorded at different times during the day in samples collected in 1992 from the Bahama Islands and the NE Caribbean Sea. This cyanobacterium is unique in that it is the only non-heterocystous diazotroph capable of N₂-fixation in daylight. Oxygen evolution was measured under conditions of natural day/night (LD, N=50), constant light (LL, N=14), and constant dark (DD, N=2×14). Photosynthesis vs intensity (P-I) relationships were calculated at various times of day, and the following parameters were used for further evaluation: photosynthesic capacity (P _max, 66 to 91 mg O₂ mg chl a ^-1 h^-1), initial slope of the P-I curve (, 0.23 to 0.27), dark respiration (R, 12 to 27 mg O₂ mg chl a ^-1 h^-1), and the intensity at which O₂ consumption is compensated by O₂ production (I _c, 78 to 160 Em^-2 s^-1). All means showed large standard deviations (for some parameters more than 200%). In some cases, these variations could be explained with a sinusoidal 24-h time course, but only the compensation point showed a significant daily variation (p0.001) in both LD and DD. The fact that the time course of I _c typical for natural conditions remains rhythmic under constant dark conditions strongly suggests a circadian regulation. Few circadian rhythms have been observed in prokaryotes, and this appears to be the first observation of such a rhythm in a cyanobacterium which fixes N₂ in daytime.     

Foraging behaviour of larval cod (<Emphasis Type="Italic">Gadus morhua</Emphasis>) at low light intensities

The ability to forage at low light intensities can be of great importance for the survival of fish larvae in a pelagic environment. Three-dimensional silhouette imaging was used to observe larval cod foraging and swimming behaviour at three light intensities (dusk ~1.36 × 10⁻³ W/m², night ~1.38 × 10⁻⁴ W/m² and darkness ~3.67 × 10⁻⁶ W/m²) at 4 different ages from 6 to 53 days post-hatch (dph). At 6 dph, active pursuit of prey was only observed under dusk conditions. Attacks, and frequent orientations, were observed from 26 dph under night conditions. This was consistent with swimming behaviour which suggested that turn angles were the same under dusk and night conditions, but lower in darkness. Cod at 53 dph attacked prey in darkness and turn angles were not different from those under other light conditions. This suggests that larvae are still able to feed at light intensities of 3.67 × 10⁻⁶ W/m². We conclude that larval cod can maintain foraging behaviour under light intensities that correspond to night-time at depths at which they are observed in the field, at least if they encounter high-density patches of prey such as those that they would encounter at thin layers or fronts.     

Ontogenetic,social, spatial and seasonal variations in condition of the reef herbivore Sparisoma viride

We studied the condition of stoplight parrot-fish, Sparisoma viride, collected from the fringing reef of Bonaire (Netherlands Antilles) between March 1987 and October 1991. To this end, we compared length-weight relationships using analysis of covariance. The condition of different life phases [juveniles, initial phase (IP) and terminal phase (TP) adults] and social categories (territorial and group adults) is compared in different seasons, taking into account spatial variability along a depth gradient. Variations in condition are related to differences in behaviour, the use of space and the distribution of food. The average length-weight relationship of fish with empty guits is described by the equation: W _Empty=9.115x10^-6xFL ^3.140 (n=386, R²=99.82%, W in g, FL in mm). Territorial TP males were found to be in poorest condition, whereas (sexually inactive) group TP showed the best and IP fish an intermediate condition. These differences are ascribed to varying investments in territory defence and reproduction, which affect condition more than the vertical distribution of food. All categories were in minimum condition between May and July, the season with longest day lengths and increasing water temperatures. This seasonal effect cannot be ascribed to increased reproductive effort and suggests that the higher energetic demands due to the longer active period of fish are not completely met by increased food uptake. It is inferred that food may be a limiting factor at times.     

Home range and social behavior of three species of European Pitymys (Mammalia,Rodentia)

Summary Habits, home range, and social behavior of three species of voles of the genus Pitymys, P. multiplex, P. subterraneus, and P. savii, were studied in Tessin (Switzerland) by radioactive tagging. P. multiplex and P. savii are fossorial and often use the burrow systems of moles (Talpa); P. subterraneus moves around on the surface under dense vegetation. Males and females of P. multiplex were territorial and their home ranges averaged 342 and 229 m² respectively. The mating system appeared to be monogamous. P. savii male and female home ranges averaged 445 and 298 m² respectively. Groups of up to one to three adult females, one or more adult males, and several young, occupied exclusive communal territories. The mating system appeared to be flexible, including monogamy, polygyny, and polyandry. P. subterraneus females occupied exclusive territories (mean 256 m²) overlapped by the home ranges of one or more males (1025 m²). The mating system appeared to be promiscuous. Individuals of the three species occupied one to seven nests. In P. savii all family members utilized three or more communal nests at the same time or alternatively. Co-nesting between males and females of P. multiplex or P. subterraneus were observed less frequently.     

Light availability and diurnal growth of a green macroalga (Caulerpa cupressoides) and a seagrass (Halophila decipiens)

The effects of daily light period on diurnal growth patterns of a green macroalga [Caulerpa cupressoides v.lycopodium f.elegans (J. Agardh) Weber-van Bosse] and a seagrass (Halophila decipiens Ostenfeld) were investigated in Salt River submarine canyon in the US Virgin Islands in summer 1984. The daily light period, in which quantum irradiance exceeded the light saturation point for photosynthesis of the macroalga and seagrass, was manipulated in situ using lamps and shades. Plant growth was measured every 6 h for 7 d under natural and experimental daily light periods.C. cupressoides grew at the same rate day and night.H. decipiens grew more during the day than at night, a pattern that persisted under continuous light and dark treatments, indicating endogenous control of diurnal growth. Growth vs daily light period curves indicate thatC. cupressoides grew faster thanH. decipiens in short daily light periods, consistent with the observation that the macroalga penetrates to deeper water than the seagrass in Salt River canyon. Overall growth (day + night) ofH. decipiens was unaffected in lengthened light periods and reduced in shortened light periods. Chlorophyll content ofC. cupressoides was not correlated with light availability, while that ofH. decipiens was positively correlated. The alga and seagrass had different diurnal growth patterns but similar overall growth responses to daily light periods. This study shows that diurnal growth patterns are probably under endogenous control, while overall growth is a response to in situ light conditions.Contribution^#193 from West Indies Laboratory and the National Undersea Research Program     

Effects of wave-induced lightflecks in the intertidal zone on photosynthesis in the macroalgae Postelsia palmaeformis and Hedophyllum sessile (Phaeophyceae)

Intertidal algae are exposed to a highly variable photic regime because of crashing waves. We measured photosynthetic rate of whole fronds of the seaweeds Postelsia palmaeformis (Ruprecht) (at Bodega Marine Laboratory, 1991) and Hedophyllum sessile (Setchell) (Phaeophyceae) (at Friday Harbor Laboratories, 1990) in flashing and steady-state photosynthetically active radiation (PAR) of equal irradiance, using a recirculating metabolism chamber designed to minimize the thickness of diffusional boundary layers on the surfaces of algal tissues. The dimensionless ratio of photosynthetic rate under flecking PAR (P_fleck) and the sum of photosynthetic rate under steady state PAR (P_s) of high and low irradiance was computed for lightfleck periods from 0.2 to 100 s. P_fleck:P_s is a measure of the light-flash utilization-efficiency in flashing light, and was greater than unity at periods between lighflecks of 2 to 30 s, with a peak at 10 s. We used a novel optical fiber irradiance meter to measure PAR incident on fronds of P. palmaeformis as they were washed about by waves breaking in the intertidal zone, and compared the light records to that obtained by a stationary sensor under the canopy. PAR flashing period was closely correlated with the period of breaking waves in stands of P. palmaeformis. We estimated the seasonal spectrum of period between light flashes in stands of this species by examining the spectral density of ocean waves at Bodega Marine Laboratory, Bodega Bay, California. The wave spectrum peaks at a period (10 s) where light-flashes may theoretically enhance the light-flash utilization-efficiency of seaweeds. We calculate that the enhanced light-flash utilization-efficiency wrought by wave-induced light-flashes may contribute to significant gains in primary productivity of these macroalgae under some conditions.     

Large males dominate: ecology,social organization,and mating system of wild cavies,the ancestors of the guinea pig

Ecological factors differently affect male and female animals and thereby importantly influence their life history and reproductive strategies. Caviomorph rodents are found in a wide range of habitats in South America and different social and mating systems have evolved in closely related species. This permits to study the impact of ecological factors on social evolution. In this study, we investigated the social organization and the mating system of the wild cavy (Cavia aperea), the ancestor of the domestic guinea pig, in its natural habitat in Uruguay. Based on our laboratory investigations, we expected a polygynous system with large males controlling access to females. Results from radiotelemetry and direct observations showed that females occupied small stable home ranges which were largely overlapped by that of one large male, resulting in a social organization of small harems. In some cases, small satellite males were associated with harems and intermediate-sized roaming males were occasionally observed on the study site. However, microsatellite analyses revealed that offspring were exclusively sired by large males of the same or neighboring harems, with a moderate degree of multiple paternity (13–27%). Thus, the mating system of C. aperea can be described as polygynous and contrasts with the promiscuous organization described for other species of cavies (Cavia magna, Galea musteloides and Microcavia australis) living under different ecological conditions. Our findings stress the strong impact of environmental factors on social evolution in Caviomorphs as resource distribution determines female space use and, thereby, the ability of males to monopolize females. Electronic supplementary material  The online version of this article (doi:) contains supplementary material, which is available to authorized users.