Photoperiodic and thermal regulation of antifreeze protein levels in the beetle Dendroides canadensis

The importance of photoperiod, temperature and their interaction in controlling the seasonal pattern of haemolymph antifreeze protein levels in larvae of the beetle Dendroides canadensis was investigated. A complete photoperiodic response curve for antifreeze protein production was generated at 20°C with larvae collected in early fall. Individuals exposed to a 10-h photoperiod or less, including constant darkness, had significantly elevated antifreeze levels over those maintained in an 11-h photoperiod or more, including constant light. The critical daylength resulting in 50% population response lies between LD 11:13 and LD 10:14. This photoperiodic response was masked at sufficiently low (threshold between 15 and 10°C) and high (threshold between 25 and 30°C) temperatures. Partial photoperiodic response curves (at 17 and 25°C) obtained within this specified temperature range indicate that the position of the critical photoperiod (between 10 and 11 h) is stable while the amplitude of the response curve is temperature dependent.Experiments investigating the mechanisms controlling the spring depletion of protein antifreeze levels suggest that both photoperiod and temperature are important.The dominant response of photoperiod in the fall along with the modifying effects of temperature are considered to provide the necessary precision to assure adequate cold tolerance early in the fall and the flexibility to protect the species from yearly variation in weather conditions.     

Time measurement in the photoperiodic induction of sexual rest in the terrestrial isopod Armadillidium vulgare (Latreille)

The photoperiodic control of sexual rest in Armadillidium vulgare was investigated using various experimental protocols. When reared in conditions of a Nanda-Hamner (i.e. resonance) protocol from their first parturial moult to their post experimental moult, females showed a weak resonance effect in sexual rest incidence. The transfer from a long day cycle to a symmetrical skeleton photoperiod--consisting of two equal light pulses per 24 h of continuous darkness--revealed the involvement of a circadian oscillatory system in the photoperiodic clock of this species. The data, obtained in the whole experiments, suggested that both oscillator and hourglass features are involved in the photoperiodic response controlling the sexual rest in Armadillidium vulgare. Moreover, when non-24-h light-dark cycles (with a long photophase) were applied, a mechanism responsible of arrest of reproduction also implied a photoperiodic counter which accumulated and added up the photoperiodic information within a sensitive period during post parturial intermoult.     

Interacting effects of photophase and scotophase on the diapause response of the Indian meal moth, Plodia interpunctella

The diapause-programming response to photoperiod in Plodia interpunctella was analyzed by exposing larvae to various 24-h and non-24-h regimes of light and darkness. The response to 24-h regimes indicated three photoperiodic parameters—a critical scotophase, a minimal photophase, and a minimal scotophase for a full expression of the response. The critical response was based on dark-time measurement, because disruption of the scotophase abolished the response and the diapause incidence varied as a function of scotophase in non-24-h regimes. The critical scotophase varied with the duration of the preceding photophase. Prevention of diapause by single or double-night interruptions of long scotophases could be explained by resetting of the dark-time measurement. The effect of a light pulse was modified by the quantitative interaction of light and dark reactions. The sensitivity to resetting by a light pulse seemed to be decreased in the early scotophase with an increasing duration of the preceding light period. Therefore, the significance of light in the photoperiodic response was something more than delimiting scotophase for the time measurement.     

Diapause induction and clock mechanism in the pine caterpillar Dendrolimus tabulaeformis (Lep., Lasiocampidae)

Abstract:  Dendrolimus tabulaeformis overwinters as third to fourth instar larvae at short days in autumn. Using 24-h light–dark cycles, the photoperiodic response curves were similar at 24 and 28°C. The critical night length was 9 h 20 min at 24°C and 9 h 50 min at 28°C. Under non-24 h light–dark cycles, duration of scotophase proved crucial in the determination of diapause. In night interruption experiments using 24-h light–dark cycle, a 1-h light pulse falling 8 h in the darkness strongly averted diapause in comparison with other light pulses. Nanda–Hamner experiments showed two weak troughs of diapause inhibition, suggesting the possible involvement of the circadian system. However, Bünsow experiments did not support the evidence of the involvement of circadian oscillatory system in photoperiodic time measurement. These results suggest that photoperiodic time measurement in this moth shows a non-oscillatory 'hourglass-like' response model or a rapidly damping oscillator model.     

Formal properties of the circadian and photoperiodic systems of Japanese quail: phase response curve and effects of T-cycles.

A role for the circadian system in photoperiodic time measurement in Japanese quail is controversial. The authors undertook studies of the circadian and photoperiodic system of Japanese quail to try to identify a role for the circadian system in photoperiodic time measurement. The circadian studies showed that the circadian system acts like a low-amplitude oscillator: It is readily reset by light without significant transients, has a Type 0 phase response curve (PRC), and has a large range of entrainment. In fact, a cycle length that is often used in resonance protocols (LD 6:30) is within the range of entrainment. The authors employed T-cycle experiments; that is, LD cycles with 6- and 14-h photoperiods and period lengths ranging from 18 to 36 h to test for circadian involvement in photoperiodic time measurement. The results did not give evidence for circadian involvement in photoperiodic time measurement: T-cycles utilizing 6-h photoperiods were uniformly noninductive (that is, did not stimulate the reproductive system), whereas T-cycles utilizing 14-h photoperiods were inductive (stimulatory). A good match was observed between the phase-angles exhibited on the T-cycles employing 6-h photoperiods and the predicted phase-angles calculated from a PRC generated from 6-h light pulses.     

Photoperiodic clock of diapause induction in Pseudopidorus fasciata (Lepidoptera: Zygaenidae)

Pseudopidorus fasciata enters diapause as fourth instar larvae at short day lengths. Using 24-h light-dark cycles, the photoperiodic response curves in this species appeared to be similar with a critical night length of 10.5h at temperatures below 30 degrees C. At an average temperature of 30.5 degrees C, the critical night length had shifted to between 15 and 17h. In experiments using non-24-h light-dark cycles, it was clearly demonstrated that the dark period (scotophase) was the decisive phase for a diapause determination. In night interruption experiments using 24-h light-dark cycles, a 1-h light pulse at LD12:12 completely reversed the long night effect and averted diapause in all treatments. At LD 9:15 light pulses of 1-h, 30- or 15-min also averted diapause effectively when both the pre-interruption (D(1)) or the post-interruption scotophases (D(2)) did not exceed the critical night length. If D(1) or D(2) exceeded the critical night length diapause was induced. The most crucial event for the photoperiodic time measurement in this species is the length of the scotophase. A 10-min light pulse placed in the most photosensitive phase reversed diapause in over 50% of the individuals. Night interruption experiments under non-24-h light-dark cycles indicated that the photoperiodic clock measured only D(1) regardless of the length of D(2), suggesting that the most inductive cycles are often those in which L+D are close to 24h. In resonance experiments, this species showed a circadian periodicity at temperatures of 24.5 or 26 degrees C, but not at 30.5 and 23.3 degrees C. On the other hand, Bünsow and skeleton photoperiod experiments failed to reveal the involvement of a circadian system in this photoperiodic clock. These results suggest the photoperiodic clock in this species is a long-night measuring hourglass and the circadian effect found in the final expression of the photoperiodic response in the resonance experiments may be caused by a disturbing effect of the circadian system in unnatural regimes.     

Metamorphic rate as a function of the light/dark cycle in Rana pipiens larvae

1. The rate of development of Rana pipiens tadpoles in spontaneous and thyroxine (T4)-induced metamorphosis was studied on light/dark (LD) cycles in which the photophase was held constant while the scotophase was progressively extended or vice versa. 2. Metamorphic rate fluctuated in both types of experiments as the LD cycle lengthened. However, the pattern of resonance differed with the length of the photophase. For example, with an 8 hr light phase, development rate slowed and then increased as the cycle was extended from 24 to to 36 hr, whereas with a 12 hr photophase the reverse took place. 3. The findings are compatible with the occurrence of a rhythm of light sensitivity in photoperiodic time measurement in this amphibian. 4. From the viewpoint of hormonal mechanisms, it is suggested that photoperiodic effects on metamorphic rate result from different patterns of melatonin secretion under the various LD cycles, since melatonin can modify the action of T4 in metamorphosis.     

Effect of Light Quality on the Circadian Expression of Nitrate Reductase in the Red Macroalga Gracilaria tenuistipitata

A circadian rhythm in the activity of nitrate reductase (NR: EC 1.6.6.1) isolated from the marine red algae Gracilaria tenuistipitata is shown to be attributable to the daily oscillation of protein levels. The experiments reported here indicate that light quality has differential effects over NR expression. In extracts of algae grown under white light : dark, red light : dark and blue light : dark cycle, the activity of NR peaks during photophase, as does photosynthesis. Staining with a monoclonal antibody (NR10), raised against NR purified from Porphyra yezoensis, shows that the amount of protein changes by a factor of about 20, with a maximum occurring during photophase when algae are submitted to white and blue light. Red light changes the circadian rhythm of NR protein levels and also inhibits its night degradation. Illumination with blue light is able to restore the NR activity as well as its protein levels only when the light irradiance was the same of the white light. Surprisingly, the red light promoted 40% induction on NR activity under the same conditions.     

Photoperiodic ovarian response in yellow-throated sparrow, Gymnorhis xanthocollis: involvement of circadian rhythm

The experiments aim to investigate the mechanism of photoperiodic time measurement during photoperiodic ovarian response of subtropical yellow-throated sparrow. Groups of the photosensitive female birds were exposed to various night-interruption cycles for a period of 35 days. These light-dark cycles consisted of a basic photophase of 6h and 1h photointerruption of the 18h dark phase in 24h cycle at different points. A control group was also placed under 7L/17D. Ovarian response was observed in the night-interruption cycles in which the photointerruption of dark phase was made 12h after the onset of basic photophase. The results are consistent with the Bünning hypothesis and indicate that an endogenous circadian rhythm is involved in photoperiodic time measurement during initiation of ovarian growth in this species.     

Daily changes in neuroendocrine control of moulting hormone secretion in the prothoracic gland of the cockroach Periplaneta americana (L.)

Time of day related changes in ecdysteroid secretion by the prothoracic gland of last instar nymphs were studied using in vitro coincubations of prothoracic glands and brains under a 12-h light:12-h dark cycle. The experiments reveal that the cells of the prothoracic gland of the cockroach nymphs do not have an endogeneous circadian oscillator determining rhythmicity of ecdysteroid secretion. PTTH release in the scotophase is responsible for the peak of ecdysteroid production during the photophase.     

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.     

Experimental evidence for a non-clock role of the circadian system in spider mite photoperiodism

In the spider mite Tetranychus urticae photoperiodic time measurement proceeds accurately in orange-red light of 580 nm and above in light/dark cycles with a period length of 20 h but not in 'natural' cycles with a period length of 24 h. To explain these results it is hypothesized that the photoperiodic clock in the spider mite is sensitive to orange-red light, but the Nanda-Hamner rhythm (a circadian rhythm with a free-running period tau of 20 h involved in the photoperiodic response) is not and consequently free runs in orange-red light. To test this hypothesis a zeitgeber was sought that could entrain the Nanda-Hamner rhythm to a 24-h cycle without inducing diapause itself, in order to manipulate the rhythm independently from the orange-red sensitive photoperiodic clock. A suitable zeitgeber was found to be a thermoperiod with a 12-h warm phase and a 12-h cold phase. Combining the thermoperiod with the long-night orange-red light/dark regime, both with a cycle length of 24 h, resulted in a high diapause incidence, although neither regime was capable of inducing diapause on its own. The conclusion is that the Nanda-Hamner rhythm is necessary for the realization of the photoperiodic response, but is not part of the photoperiodic clock, because photoperiodic time measurement takes place in orange-red light whereas the rhythm is not able to 'see' the orange-red light. It is speculated that the Nanda-Hamner rhythm is involved in the timely synthesis of a substrate for the photoperiodic clock in the spider mite.     

Evaluation of the Frequency Demultiplication Hypothesis of Circannual Pupation Rhythm in the Varied Carpet Beetle Anthrenus verbasci (Coleoptera: Dermestidae)

The present study was reported to examine whether the circannual pupation rhythm in Anthrenus verbasci is derived from a circadian rhythm through a process of frequency demultiplication. This frequency demultiplication hypothesis requires that the period of the circannual rhythm is proportional to the period of the entrained circadian rhythm. When larvae were reared under constant photoperiods of T = 20h, 22h, 24h and 26h at 20°C, the larval duration differed among the photoperiodic conditions, although there was no positive correlation between the period of T cycle and larval duration. The differences among photoperiods may have been caused by the duration of the photophase. Therefore, the results did not support the frequency demultiplication hypothesis.     

Photoperiodism of diapause induction in Thyrassia penangae (Lepidoptera: Zygaenidae)

Thyrassia penangae enters winter diapause as a prepupa in a cocoon. Photoperiodism of diapause induction was systematically investigated in this moth. The photoperiodic response curves under 24-h light-dark cycles showed that this insect is a typical long-day species. The critical daylength was 13 h 30 min at 25 °C, 13 h at 30 °C and 12 h 20 min at 28 °C. Transferring experiments from a short day (LD 12:12) to a long day (LD 15:9) or vice versa indicated that photoperiodic sensitivity mainly occurs during the larval period. In experiments using non-24-h light-dark cycles, when the length of photophase exceeded the critical daylength (13.5 h), was diapause inhibited effectively, even when the length of scotophase exceeded the critical nightlength (10.5 h). Only when a long scotophase was combined with a short photophase, diapause was induced effectively. This result suggests that daylength measurement is more important than nightlength measurement in T. penangae. Night interruption experiments under 24-h light-dark cycles exhibited two points of apparent light sensitivity, but the photosensitive position was highly influenced by temperature and the length of scotophase. Nanda-Hamner experiments failed to reveal the involvement of a circadian system in this photoperiodic time measurement. All light-dark cycles from LD 12:12 to LD 12:72 resulted in a short day response, and all cycles from LD 14:4 to LD 14:72 resulted in a long day response, suggesting that photoperiodic time measurement in this moth is performed by a day-interval timer or an hourglass-like clock.     

Effect of light intensity on the oviposition rhythm of the altitudinal strains of Drosophila ananassae

The sensitivity of the circadian photoreceptors mediating entrainment of the eclosion rhythm and phase shifts of oviposition rhythm of the high altitude (HA) strain of Drosophila ananassae originating from Badrinath (5123 m above sea level) in the Himalayas was compared with the low altitude (LA) strain from Firozpur (179 m above sea level). Reduced photic sensitivity of the HA strain is regarded as the result of natural selection, which led to the weakening of the coupling mechanism between the circadian pacemaker and light at the high altitude of origin. The present study was designed to determine whether or not the photic entrainment of the oviposition rhythm of the HA strain of D. ananassae is also altered by the high altitude of its origin, and the results are compared with those of the LA strain. The effects of light intensity on the phase angle difference (Ψ), degree of rhythmicity (R), the percent oviposition in photophase, the threshold light intensity (i.e., the intensity at which stable entrainment occurred), and the saturation light intensity (i.e., the intensity beyond which the values of Ψ or amplitude of rhythm remained unaltered) were determined. Entrainment was studied in light-dark cycles in which the light intensity of 12 h of photophase varied from 1 to 1000 lux, and complete darkness prevailed in all scotophases. The oviposition rhythm of the HA strain was arrhythmic from 1 to 90 lux, weakly rhythmic at 95 lux, but rhythmic at or above 100 lux, while that of the LA strain was weakly rhythmic at 1 lux but rhythmic at or above 2 lux. Oviposition of the HA strain occurred mostly in the photophase, while that of the LA strain occurred in the scotophase; as a result, the oviposition medians of the HA strain were around the subjective forenoons while those of the LA strain were around the subjective evenings. The percent of oviposition in photophase increased from 68 to 98 in the HA strain and from 5 to 33 in the LA strain as light intensity increased from 1 to 1000 lux. In the HA strain, the Ψ values were significantly less and values of R and percent oviposition in photophase were significantly more than those of the LA strain at each level of light intensity. Threshold and saturation intensities for Ψ were 100 and 700 lux, respectively, for the HA strain, but just 2 and 45 lux, respectively, for the LA strain. The saturation intensity for R was 650 and 700 lux for the HA and LA strains, respectively. These results extend the confirmation that the reduced photic sensitivity of the HA strain might have been acquired through natural selection in response to environmental conditions at the high altitude of its origin.     

External coincidence and photoperiodic time measurement in the spider mite Tetranychus urticae

The incidence of diapause in the spider mite Tetranychus urticae was predicted for various photoperiodic regimes, according to the external coincidence model of photoperiodic time measurement. A phase response curve was constructed for the hypothetical photoperiodic oscillator in these mites: entrainment of this photoperiodic oscillator to a variety of ‘complete’ and ‘skeleton’ photoperiods was calculated using a transformation method for circadian rhythms. The external coincidence model proved adequate to describe experimental results with T. urticae in ‘complete’ photoperiods (T = 24 hr), symmetrical ‘skeleton’ photoperiods (T = 24 hr), asymmetrical ‘skeleton’ photoperiods (T = 24 hr) (night-interruption experiments), and ‘resonance’ experiments, in which the light component of a light/dark cycle was held constant at 8 hr and the dark component was varied over a wide range in successive experiments, providing cycles with period lengths up to 92 hr. The external coincidence model proved inadequate to explain results obtained in a ‘T-experiment’ with T. urticae comprising 1 hr pulses of light in a cycle of LD1:17.5 (T = 18.5 hr) with the first pulse of the train starting at different circadian phases. The validity and limitations of the external coincidence model as an explanation of photoperiodic time measurement in T. urticae are discussed in view of the above results.     

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.     

Circadian Protection against Reactive Oxygen Species Involves Changes in Daily Levels of the Manganese- and Iron-Containing Superoxide Dismutase Isoforms in Lingulodinium polyedrum

A circadian rhythm in the total activity of superoxide dismutase (SOD; EC 1.15.1.1) from the unicellular alga Lingulodinium polyedrum is shown to be attributable to the mitochondrial MnSOD and chloroplastic FeSOD isoforms. Activity gels and labelling with polyclonal antibodies against pure CuZnSOD, MnSOD and FeSOD revealed a distinct circadian pattern in the abundance of the latter two isoforms, with peak values in early photophase 5 times greater than at the dark phase. However, no such changes were detected for the CuZnSOD isoform, which remained at constant levels over the 24-h light/dark cycle. These SOD isoforms might provide protection against damage from photochemically generated oxygen radicals, thus preventing subcellular oxidative stress.     

Circadian basis of photoperiodically induced testicular growth in redheaded bunting, Emberiza bruniceps

Short day (8L : 16D), pretreated adult male redheaded buntings were held on various light—dark cycles of 20 to 30 h duration, in which a fixed ultra-short photophase of 3 h was combined with scotophases of varying duration. A photoperiodic testicular response was obtained only in 28- and 30-h cycles (3L : 25D and 3L : 27D). The same photo-period (3 h) in 20- to 26-h cycles (3L : 17D, 3L : 19D, 3L : 21D and 3L : 23D) failed to stimulate testicular growth. The results can be interpreted on the assumption that the positive testicular response in this species, under ultra-short-day light cycles, is the result of an advance in the photosensitive phase of the photoperiodic response system so that it coincides at least partly with the external photophase. The results thus appear to conform with the Bünning hypothesis or external coincidence model.     

Temperature dependent eclosion rhythmicity in the high altitude Himalayan strains of Drosophila ananassae

The circadian pacemaker controlling the eclosion rhythm of the high altitude Himalayan strains of Drosophila ananassae captured at Badrinath (5123 m) required ambient temperature at 21°C for the entrainment and free-running processes. At this temperature, their eclosion rhythms entrained to 12h light, 12h dark (LD 12:12) cycles and free-ran when transferred from constant light (LL) to constant darkness (DD) or upon transfer to constant temperature at 21°C following entrainment to temperature cycles in DD. These strains, however, were arrhythmic at 13 or 17°C under identical experimental conditions. Eclosion medians always occurred in the thermophase of temperature cycles whether they were imposed in LL or DD; or whether the thermophase coincided with the photophase or scotophase of the concurrent LD 12:12 cycles. The temperature dependent rhythmicity in the Himalayan strains of D. ananassae is a rare phenotypic plasticity that might have been acquired through natural selection by accentuating the coupling sensing mechanism of the pacemaker to temperature, while simultaneously suppressing the effects of light on the pacemaker.