Circadian nature of the photoperiodic clock in Japanese quail

Summary The photoperiodic clock in quail (Coturnix colurnix japonica) is based upon a rhythm of photoinducibility (Øi) but the extent to which this rhythm is circadian remains unclear. Two types of experiment investigated this situation. In the first, gonadectomized quail were adapted to live in periods of darkness by training them on a schedule containing one short day and 3 days of darkness (SD/DD/DD/DD). They were then exposed to a single pulse of 6 or 10 h of light at different times across 3 days of darkness. The photoperiodic response, measured by the increase in LH secretion, showed clear rhythmicity, demonstrating unequivocally the circadian nature of Øi. The second set of experiments employed Nanda-Hamner cycles and varied the length of the photoperiod from 6 to 11 h. Responsiveness in a 36 h or a 60 h cycle was highly dependent upon the length of the photoperiod, something not predicted from theory. For instance, LD 6:30 was not photoperiodically inductive but LD 10:26 was clearly inductive. Close analysis of patterns of LH secretion indicated an unexpected delay before induction occurred and then a rapid rise to a stable level of induction. When LH was measured in every pulse under LD 10:26 there was no evidence that LH levels alternately increased and decreased. This is not consistent with the simplest interpretation of Nanda-Hamner experiments where alternate pulses of light are thought to entrain the rhythm or induce a photoperiodic response by coinciding with Øi. It is concluded that the quail's photoinducible rhythm is indeed based on a circadian rhythm but one that is only weakly self-sustaining. Possibly as a consequence of this, the rhythm's behaviour under abnormal photoperiodic cycles may be rather different from that found in other species and from other circadian rhythms in quail.Abbreviations Øi photoinducible phase - LH luteinizing hormone     

Determination of effective light pulse and classical Bünsow experiment in the larval diapause of the Indian meal moth Plodia interpunctella

Plodia interpunctella Hübner (Lepidoptera: Pyralidae) comprises a model insect to analyse the photoperiodic time‐measuring system controlling its larval diapause. In the present study, the effective length of light pulse in night interruption experiments is determined at 25 °C. Various lengths of light pulse are tested by inserting them at the midnight of an LD 12 : 12 h photoperiod. When the light pulse is 15 or 30 min, the incidence of diapause is 86%. To inhibit the induction of diapause effectively, a light pulse of 1.75–2 h is needed. The incidence of diapause is 12% under an LD 12 : 5 : 2 : 5 h photoperiod. To determine the precise role of the light pulse, 2‐h light pulses placed at the midnight of an LD 12 : 12 h photoperiod are disrupted systematically by darkness. When a 2‐h light pulse is disrupted by 15 min of darkness, diapause is generally prevented (< 29%) regardless of the temporal position of darkness. Longer disruption by darkness induces diapause moderately (37–67%). A Bünsow experiment is also conducted at 25 and 20 °C, in which the main photophase of 12 h of light is combined with 24–72‐h scotophases scanned by a 2‐h light pulse. The photoperiodic cycle length tested, therefore, varies in the range 36–84 h. In each cycle length, the incidence of diapause fluctuates as the light pulse moves toward dawn. However, no regular and circadian changes in the percentage diapause are observed in relation to diapause determination.     

Entrainment Properties of the Locomotor Activity Rhythm of Drosophila melanogaster Under Different Photoperiodic Regimens

In this paper we report the results of an experiment to assess how closely repeated brief light pulses (LPs) mimic the effects of 12:12 h light/dark (LD) cycles (PPc). The locomotor activity rhythm of individual fruit flies from a laboratory population of Drosophila melanogaster was monitored under four different photoperiodic regimens, created using 12 h of light and 12 h of darkness or brief light pulses (LPs). The phase relationship (Ψ) and the stability (precision) of the locomotor activity rhythm during entrainment were estimated in order to compare the state of the circadian clocks under the four different photoperiodic regimens. The flies (n = 72) were subjected to four different LD cycles: (i) 12 h of light and 12 h of darkness (complete photoperiod, PPc); (ii) a single brief LP of 15 min duration presented close to the onset of activity (SLP-1); (iii) a single brief LP of 15 min duration administered close to the offset of activity (SLP-2); and (iv) two brief LPs administered 12 h apart (skeleton photoperiod, PPs). The locomotor activity rhythm of the flies was first monitored under constant darkness (DD) for about 10 days and then under the four different photoperiodic regimens for about 10 days, and finally in DD for the remainder of the experiment. The Ψ of the locomotor activity rhythm and its precision under PPc and PPs did not differ significantly, but they were significantly different from the SLP-1 and SLP-2 conditions. The results provide interesting insights into photoentrainment mechanisms of circadian clocks in D. melanogaster, and suggest that skeleton photoperiods, but not single brief LPs, mimic the actions of complete photoperiods.     

Effect of temperature on photoperiodic response in a selected 'non-diapause' strain of Pyrrhocoris apterus (Heteroptera)

Abstract. The artificially selected 'non-diapause' strain of Pyrrhocoris apterus (L.) (Heteroptera) showed no diapause response to photoperiod at 26°C (Socha & Hodkova, 1994). However, the diapause response to short-day photoperiod (LD 12:12 h) became apparent at lower temperatures of 17°C (70% diapause) or 20°C (41% diapause). Diapause was induced in 60% females by short-day photoperiod combined with thermoperiod of 26/16°C, whereas only 20% diapause was induced by the same thermoperiod under continuous darkness. Thus the time-measuring system was not removed by artificial selection but the diapause response was shifted to lower temperatures. The diapause response to short days seems to be favoured rather by low temperature during scotophase than by low temperature throughout the whole light/dark cycle. If the percentage of diapause at 26°C is compared in F₁ hybrids and in wild and selected parental strains the diapause appears to be dominant at LD 13:11 h but recessive at LD 11:13 h and LD 10:14 h. A hypothesis is proposed that the inheritance of the percentage of diapause in F1 hybrids is determined by interactions of genes controlling the temperature dependence of photoperiodic response.     

Why is the number of days required for induction of adult diapause in the linden bug Pyrrhocoris apterus fewer in the larval than in the adult stage?

Adult females of Pyrrhocoris apterus, programmed for diapause by short-day (SD) photoperiod and those programmed for reproduction by long-day (LD) retain photoperiodic information in continuous darkness (DD) until death. However, if the interruption of SD by DD is made in the course of diapause programming in adults, then the incidence of diapause depends on the number of SD cycles received before DD, with no evidence that the photoperiodic clock is free-running at DD to complete diapause induction. These results indicate that the photoperiodic clock is stopped after transfer to DD and the information accumulated before transfer to DD is maintained. Diapause programming in the adult stage requires 9–10 SD cycles to induce diapause in 80% of individuals. However, if the diapause programming starts after ecdysis of LD-larvae to the last instar, only 3 SD cycles before transfer to DD are required for diapause in 80% of individuals. Surprisingly, if the newly ecdysed last instar LD-larvae, sensitive to photoperiod, are transferred to DD (thus they did not experience any SD), diapause occurs in 40% of the individuals. Thus, diapause ‘information’ is present in LD-larvae and is responsible for a lower number of SD required for diapause induction in the larval than in the adult stage.     

Clock gene daily profiles and their phase relationship in the rat suprachiasmatic nucleus are affected by photoperiod

Rhythmicity of the rat suprachiasmatic nucleus (SCN), a site of the circadian pacemaker, is affected by daylength; that is, by the photoperiod. Whereas various markers of rhythmicity have been followed, so far there have been no studies on the effect of the photoperiod on the expression of the clock genes in the rat SCN. To fill the gap and to better understand the photoperiodic modulation of the SCN state, rats were maintained either under a long photoperiod with 16 h of light and 8 h of darkness per day (LD16:8) or under a short LD8:16 photoperiod, and daily profiles of Per1, Cry1, Bmal1 and Clock mRNA in darkness were assessed by in situ hybridization method. The photoperiod affected phase, waveform, and amplitude of the rhythmic gene expression as well as phase relationship between their profiles. Under the long period, the interval of elevated Per1 mRNA lasted for a longer and that of elevated Bmal1 mRNA for a shorter time than under the short photoperiod. Under both photoperiods, the morning and the daytime Per1 and Cry1 mRNA rise as well as the morning Bmal1 mRNA decline were closely linked to the morning light onset. Amplitude of Per1, Cry1, and Bmal1 mRNA rhythms was larger under the short than under the long photoperiod. Also, under the short photoperiod, the daily Clock mRNA profile exhibited a significant rhythm. Altogether, the data indicate that the whole complex molecular clockwork in the rat SCN is photoperiod dependent and hence may differ according to the season of the year.     

Photoperiodic control of rat pineal serotonin N-acetyl-transferase activity

Adult male albino rats were acclimated to constant light (light:dark-LD-24:0) or to darkness interrupted with brief periods of light at 6 h intervals (LD 1/4:5 3/4 X 4) concurrently with rats maintained in a LD 14:10 photoperiodic cycle. The activity and rhythmicity of pineal serotonin N-acetyltransferase (NAT) was examined at regular intervals for 24 hours in rats maintained in the experimental photoperiods and compared to pineal NAT activity and rhythmicity in rats maintained in the LD 14:10 photoperiod. The results indicate that constant light is capable of depressing nocturnal levels of rat pineal NAT and obliterating the pineal NAT rhythm. Likewise, rats subjected to darkness interrupted with brief periods of light at 6 h intervals experienced a similar response in pineal NAT activity to animals subjected to constant light, i.e., pineal NAT activity was persistently low and the rhythmicity was obliterated. The results are discussed relative to the hypothesis that the pineal NAT activity responds to an endogenous rhythm in photoperiodic time measurement. The evidence herein suggests that the time of occurrence of environmental light in the photoperiod is more important in determining pineal NAT activity and/or rhythmicity than is the total amount of darkness or the dark to light ratio to which animals may be subjected.     

Responsiveness to photoperiodic changes in the circannual rhythm of the varied carpet beetle, <Emphasis Type="Italic">Anthrenus verbasci</Emphasis>

The circannual pupation rhythm of Anthrenus verbasci is entrained to an environmental cycle by changes in photoperiod. Exposure of larvae reared under short-day conditions to 4 weeks of long days can induce phase-dependent phase shifts. In the present study, we examined the range of photoperiodic changes effective for phase shifts at 20°C. For larvae under light/dark (LD) 12:12 conditions, 4-week exposure to LD 14:10 caused a clear phase delay, as great an extent as that brought about by exposure to LD 15:9 and LD 16:8. In contrast, the delay brought about by exposure to LD 13:9 was slight. For larvae under LD 10:14, exposure to LD 14:10 and LD 16:8 for 4 weeks induced a phase delay, but exposure to LD 12:12 did not. These results indicate that a clear phase delay is induced when the photoperiodic change exceeds a critical value in the photophase between 13 and 14 h, regardless of the amplitude of the change. Although phase advances were smaller than phase delays, they depended on the amplitude of photoperiodic changes rather than the absolute photophase duration in contrast to the case of the phase delay.     

The non-photic induction of spermatogenic development in European starlings

Detailed studies of the photosexual biology of male European starlings (Sturnus vulgaris) document a non-obligatory involvement of photoperiod in the induction of testicular metamorphosis. Although post-winter solstice increases in daily photophase duration are responsible for the ecologically correct chronology of the annual reproductive cycle, starlings maintained in the absence of daily photostimulation under go testicular metamorphosis with complete spermatogenic development. Present experiments reveal that the rate of testicular growth in starlings held in constant darkness (DD) is affected by previous photoperiodic experience. Birds held under a natural northtemperate zone photoperiod and transferred to DD on 13 September require significantly fewer days to achieve spermatogenic testes than birds pretreated under 12-and 14-h photoperiods or in constant light (LL). Complete spermatogenesis in the 14-h group is achieved only after a greater duration of DD exposure than in all other birds. Variations in the extent of the 12-h pretreatment period do not alter the testis growth rate in starlings subsequently transferred to DD. It is suggested that photoperiodic conditions applied prior to the initiation of DD treatment may affect the characteristics of circadian oscillations that occur in the absence of a photoperiodic zeitgeber, and thus change the reproductive response rate through alterations of hormonal secretions from the hypothalamo-hypophyseal axis.Presented at the Eighth International Congress of Biometeorology, 9–14 September 1979, Shefayim, Israel.     

The effect of temperature on the photoperiodic 'clock' and 'counter' of a Scottish clone of the vetch aphid, Megoura viciae

Photoperiodic response curves were determined for a Scottish clone of the vetch aphid, Megoura viciae Buckton, at three temperatures: 12.5, 15, and 17.5 degrees C. Critical night lengths (CNLs) for ovipara (sexual female) induction were 6 h, 7 h and 8 h, respectively. High incidences of ovipara production were observed in all night lengths longer than the CNL including continuous darkness (DD), as well as in continuous light (LL) at 12.5 and 15 degrees C. At the same three temperatures, the number of long- or short-night cycles required for half of the experimental aphids to be ovipara producers (i.e. the required day number, RDN) was determined. The RDN for long-night cycles (LD12:12) could not be determined at 12.5 degrees C, but was temperature compensated between 15 and 17.5 degrees C. The RDN for short-night cycles (LD20:4) could not be determined at any temperature. However, as induction of oviparae was always 100% in 12.5 degrees C, 94-100% in 15 degrees C and dropped from 100% to between 47 and 71% in 17.5 degrees C, it seems that short-night accumulation was temperature dependent. When fourth-stadium larvae were transferred from LD20:4 at 20 degrees C to the same light-dark cycle at 15 degrees C, the aphids, when adult, switched to the production of oviparae after about 4 weeks. First-born progeny kept in LD20:4 and 15 degrees C switched to the production of oviparae about 7 days after the moult to adult. Thus, the photoperiodic response can be directly affected by temperature, irrespective of photoperiod. Model-generated response curves using the 'double circadian oscillator model' for photoperiodic time measurement (Vaz Nunes, M., 1998. A double circadian oscillator model for quantitative photoperiodic time measurement in insects and mites. Journal of Theoretical Biology 194, 299-311) closely resembled the observations. Differences between these data and the results of previous experiments with an English clone of M. viciae could be accounted for by differences in the photoperiodic clocks (damping rate and period) as well as the photoperiodic counters.     

Effect of a cranium-directed daily illumination cycle on the laying rhythm in Japanese quail

This study tests the effect on the laying rhythm of a light cycle reaching directly the encephala via a diode in Japanese quail maintained in constant darkness. In DD, all the birds expressed their free-running laying rhythm (period close to 25 h). When the diode is switched on 14 h per 24 h cycle, females showed the same organization as in LD with the same laying time. Thus, a photoperiodic cycle, where light was only perceived through the skull of the female quail, could synchronize its laying rhythm. This device with a LED is an interesting alternative solution to eye-patching or blinding of birds.     

Circadian rhythms of oviposition and feeding activity in Japanese quail: effects of cyclic administration of melatonin

The aim of these experiments was to test the effect of a cyclic administration of melatonin, by mimicking the daily rhythm of hormone levels, on the circadian organization of two distinct functions in quail: oviposition and feeding activity. Laying and feeding rhythms under photoperiodic conditions and constant darkness (DD) were investigated. Under DD, where the two rhythms were free running, a daily rhythm of melatonin was administered. In LD 14h:10h, two different individual profiles of laying were established, with stable females laying at the same time each day and delayed females laying progressively later each day. For feeding activity, all birds were clearly synchronized to the photoperiodic cycle. In DD, the laying birds showed a free-running rhythm of oviposition with a period longer than 24 h for both profiles but the delayed profile females had a longer period than stable profile females. In comparison, the free-running period of feeding rhythm of the same birds was shorter than 24 h. A cyclic administration of melatonin had no effect on laying rhythm, which continued to free-run in DD, whereas feeding activity was synchronized as soon as the first cycle of melatonin was administered. From these results, it seems that two different circadian systems drive each of the two types of behavior separately. Melatonin could be the main synchronizer for the temporal control of feeding behavior, but it does not play a part in the control of oviposition in Japanese quail.     

Effects of bisphenol A and light conditions on the circadian rhythm of the goldfish Carassius auratus

We investigated how exposure to bisphenol A (BPA) under different photoperiodic conditions affected the expression of clock genes in the brain and liver of the goldfish, Carassius auratus. Three photoperiodic conditions were used: control, LD; continuous light, LL; and continuous dark, DD; the fish were exposed to three concentrations of BPA, namely 0, 10, or 100 μg/L. We measured changes in the expression of cryptochrome 1 (Cry1), period 2 (Per2), and melatonin receptor 1 (MT-R1). The levels of Cry1, Per2, and MT-R1 mRNAs decreased with increasing BPA concentration and with increasing exposure time. Expression of Cry1 and Per2 increased more in the LL group than in the LD and DD groups. However, for MT-R1, the DD group showed increased expression compared to the LL and LD groups. Our analysis shows that circadian rhythms in goldfish can be disrupted by exposure to BPA and that the response can be modified by regulating the photoperiod.     

Seasonality in a temperate zone bird can be entrained by near equatorial photoperiods

Birds use photoperiod to control the time of breeding and moult. However, it is unclear whether responses are dependent on absolute photoperiod, the direction and rate of change in photoperiod, or if photoperiod entrains a circannual clock. If starlings (Sturnus vulgaris) are kept on a constant photoperiod of 12h light:12h darkness per day (12L:12D), then they can show repeated cycles of gonadal maturation, regression and moult, which is evidence for a circannual clock. In this study, starlings kept on constant 11.5L:12.5D for 4 years or 12.5L:11.5D for 3 years showed no circannual cycles in gonadal maturation or moult. So, if there is a circannual clock, it is overridden by a modest deviation in photoperiod from 12L:12D. The responses to 11.5L:12.5D and 12.5L:11.5D were very different, the former perceived as a short photoperiod (birds were photosensitive for most of the time) and the latter as a long photoperiod (birds remained permanently photorefractory). Starlings were then kept on a schedule which ranged from 11.5L:12.5D in mid-winter to 12.5L:11.5D in mid-summer (simulating the annual cycle at 9 degrees N) for 3 years. These birds entrained precisely to calendar time and changes in testicular size and moult were similar to those of birds under a simulated cycle at 52 degrees N. These data show that birds are very sensitive to changes in photoperiod but that they do not simply respond to absolute photoperiod nor can they rely on a circannual clock. Instead, birds appear to respond to the shape of the annual change in photoperiod. This proximate control could operate from near equatorial latitudes and would account for similar seasonal timing in individuals of a species over a wide range of latitudes.     

Arylalkylamine N-acetyltransferase gene expression in retina and pineal gland of rats under various photoperiods

The present study examines how the circadian oscillators in the retina and the suprachiasmatic nucleus (SCN) respond to changes in photoperiod. Arylalkylamine N-acetyltransferase (aa-nat) gene expression studied by quantitative RT-PCR revealed that in adult Sprague-Dawley rats kept under different light-dark (LD) cycles for two weeks the temporal pattern of AA-NAT mRNA expression was identical in retina and pineal gland. In both tissues, the time span between the onset of darkness and the nocturnal rise in AA-NAT mRNA expression was 3 h under LD 20:4, 6 h under LD 12:12, and 15 h under LD 4:20. As aa-nat expression in the pineal gland is regulated by the circadian oscillator in SCN, the results suggest that the photoperiodic differences accompanying the seasons of the year are imprinted in more than one oscillator and that this may accentuate the important message regarding 'time of year.'     

Responses to stepwise photoperiodic changes for the larval diapause of the Indian meal moth Plodia interpunctella

Abstract The Indian meal moth Plodia interpunctella Hübner (Lepidoptera: Pyralidae) diapauses as a last‐instar (fifth) larva. At 30 °C, no larvae enter diapause under any photoperiodic conditions; at 25 °C, the photoperiodic response curve is a long‐day type with a critical length of approximately 13 h light; at 20 °C, diapause is induced moderately even under long days (> 13 h). Cumulative effects of short days or long days on diapause induction are determined by alternate, stepwise and gradually changing regimes of photoperiod at 25 °C. When the larvae are repeatedly exposed to LD 16 : 8 h and LD 12 : 12 h photoperiods every other day, the incidence of diapause is 37%. When the larvae are placed under an LD 16 : 8 h photoperiod for 2 days and then under an LD 12 : 12 h photoperiod for 1 day, it is 38 %. Exposure to an LD 16 : 8 h photoperiod for 1 day and then to an LD 12 : 12 h photoperiod for 2 days induces only 15% diapause. This may indicate that the photoperiodic information is not accumulated in a simple fashion despite the generally accepted hypothesis (i.e. photoperiodic counter). Larvae exposed to an LD 16 : 8 h photoperiod for 5 days after oviposition express a very high incidence of diapause even under short days between an LD 2 : 22 h and LD 12 : 12 h photoperiod. After 10 days exposure to an LD 16 : 8 h photoperiod, however, the short day does not induce diapause strongly. On the other hand, an LD 12 : 12 h photoperiod in the early larval life is highly effective in the induction of diapause. A gradual increase or decrease of photoperiod (2 min day^?1) shows that the direction of photoperiodic change does not affect the diapause determination.