A physiological model of a circannual oscillator

Recent evidence based on studies in hypothalamo-pituitary disconnected Soay sheep suggests that the generation of circannual rhythms may be local to specific tissues or physiological systems. Now, the authors present a physiological model of a circannual rhythm generator centered in the pituitary gland based on the interaction between melatonin-responsive cells in the pars tuberalis that act to decode photoperiod, and lactotroph cells of the adjacent pars distalis that secrete prolactin. The model produces a self-sustained, circannual rhythm in endocrine output that the authors explore by mathematical modeling. The circannual oscillation requires a delayed negative feedback mechanism. The authors highlight specific features of the pituitary dynamics as a guide to future research on circannual rhythms.     

Circannual rhythms of ground squirrels: a test of the frequency demultiplication hypothesis

The frequency demultiplication hypothesis (FDH) posits that circannual rhythms are generated from circadian cycles by frequency transformation to the lower-frequency rhythm. To test the FDH, we determined the periods of the circannual body mass and estrous cycles of golden-mantled ground squirrels with circadian locomotor activity rhythms entrained to 23-, 24-, or 25-hr days (T-cycles). Circannual period length did not differ among squirrels entrained to the different T-cycles; intergroup ranges were 298-314 days and 303-312 days, respectively, for body mass and estrus. These results are not consistent with the FDH and suggest instead that separate mechanisms generate circadian and circannual rhythms. In ground squirrels the circannual system influences circadian organization, but a reciprocal influence of circadian on circannual rhythms has yet to be demonstrated.     

Pinealectomy and LL Abolished Circadian Perching Rhythms but Did Not Alter Circannual Reproductive or Fattening Rhythms in Finches

In the subtropical finch, spotted munia (Lonchura punctulata) circannual rhythms (of gonads, fattening, feeding) have been demonstrated in an information-free environment of continuous illumination (LL), rendering it an ideal model for research on the physiology of the circannual clock. In an attempt to understand the involvement, if any, of the circadian system in the genesis of circannual rhythms, we studied the effect of pinealectomy (LL 15 lux) and strong continuous illumination (LL 300 lux), both known to abolish circadian rhythms, on the circadian perch-hopping rhythm and on the circannual rhythm of reproduction and fattening in the same birds. While both pinealectomy and LL 300 lux treatments abolished the circadian rhythm of motor activity, they had no effect on the circannual rhythms of gonadal size and fattening. If the endogenous circadian rhythm in perch-hopping can be taken to reflect the circadian clock mechanism associated with gonadal functioning, present results suggest that circannual rhythm of reproduction in spotted munia is independent of circadian events.     

Pinealectomy and LL Abolished Circadian Perching Rhythms but Did Not Alter Circannual Reproductive or Fattening Rhythms in Finches

In the subtropical finch, spotted munia (Lonchura punctulata) circannual rhythms (of gonads, fattening, feeding) have been demonstrated in an information-free environment of continuous illumination (LL), rendering it an ideal model for research on the physiology of the circannual clock. In an attempt to understand the involvement, if any, of the circadian system in the genesis of circannual rhythms, we studied the effect of pinealectomy (LL 15 lux) and strong continuous illumination (LL 300 lux), both known to abolish circadian rhythms, on the circadian perch-hopping rhythm and on the circannual rhythm of reproduction and fattening in the same birds. While both pinealectomy and LL 300 lux treatments abolished the circadian rhythm of motor activity, they had no effect on the circannual rhythms of gonadal size and fattening. If the endogenous circadian rhythm in perch-hopping can be taken to reflect the circadian clock mechanism associated with gonadal functioning, present results suggest that circannual rhythm of reproduction in spotted munia is independent of circadian events.     

Melatonin Entrainment of Circannual Rhythms

A melatonin‐based photoperiod timing mechanism and a circannual rhythm‐generating system interact to govern seasonal cycles in physiology and behavior in many vertebrates. This paper focuses on the pars tuberalis (PT) of the mammalian pituitary gland as a model melatonin‐responsive tissue to investigate the molecular basis of these two basic long‐term timing processes.     

Circannual rhythms in birds

In many birds, reproduction, molt, migration and other seasonal activities are controlled by endogenous circannual rhythmicity. Under constant conditions, this rhythm persists for many cycles with a period deviating from 12 months. Whether or not the rhythm is expressed depends on day length (photoperiod), which thus represents an important permissive factor in the process of rhythm generation. In nature, circannual rhythms are usually synchronized by the seasonal changes in photoperiod. However, equatorial birds may use daytime light intensity, which changes with the annual cycle of dry and rainy seasons, as a synchronizing zeitgeber. Photoperiod also modulates the rate of progress of the successive phases of the rhythmicity, such that an optimal adjustment to the annual environmental cycle is guaranteed. Populations of a given species may differ in their responsiveness to photoperiod in a manner that can be described as 'adaptive population-specific reaction norms'. In young migratory songbirds a circannual program determines changes in migratory direction and, at least partly, the time course and distance of migration. This circannual mechanism is replaced or supplemented in older birds by mechanisms formed on the basis of learning and memory. In general, circannual rhythms are intimately involved in the seasonal organization of a bird's behavior, providing the substrate onto which seasonal environmental factors act.     

A phase response curve for circannual rhythm in the varied carpet beetle <Emphasis Type="Italic">Anthrenus verbasci</Emphasis>

We know that entrainment, a stable phase relationship with an environmental cycle, must be established for a biological clock to function properly. Phase response curves (PRCs), which are plots of phase shifts that result as a function of the phase of a stimulus, have been created to examine the mode of entrainment. In circadian rhythms, single-light pulse PRCs have been obtained by giving a light pulse to various phases of a free-running rhythm under continuous darkness. This successfully explains the entrainment to light-dark cycles. Some organisms show circannual rhythms. In some of these, changes in photoperiod entrain the circannual rhythms. However, no single-pulse PRCs have been created. Here we show the PRC to a long-day pulse superimposed for 4 weeks over constant short days in the circannual pupation rhythm in the varied carpet beetle Anthrenus verbasci. Because the shape of that PRC closely resembles that of the Type 0 PRC with large phase shifts in circadian rhythms, we suggest that an oscillator having a common feature in the phase response with the circadian clock, produces a circannual rhythm.     

Synchronization of the circannual reproductive rhythm of the ewe by discrete photoperiodic signals

Although many species display endogenous circannual rhythms of biological activity that are synchronized by day length, the specific photoperiodic requirements for synchronizing such rhythms are not established for any species. We tested the hypothesis that the circannual reproductive rhythm of sheep can be synchronized by exposure to just one or two discrete blocks of photoperiodic information each year. Ewes were pinealectomized to prevent their ability to transduce photoperiodic information into altered reproductive neuroendocrine activity. During the 53/4 yr following pinealectomy, specific photoperiodic signals were restored for discrete periods of time via replacement of 24-h patterns of melatonin, the pineal hormone that transmits photic information to the reproductive neuroendocrine axis. The ewes were kept in a 12-mo photoycycle that alternated between short (8L:16D) and long (16L:8D) days every 6 mo and that was 6 mo out of phase with the geophysical year. Pineal-intact control ewes exhibited synchronous annual reproductive cycles. Noninfused pinealectomized control ewes did not exhibit synchronous cycles. Pinealectomized ewes infused with alternating 70-day blocks of short- and long-day patterns of melatonin every 6 mo for the first 21/2 yr of the experiment exhibited synchronous annual reproductive cycles that were 6 mo out of phase with those of ewes maintained outdoors. This synchrony persisted when the frequency of the melatonin treatment was reduced to just one 70-day block of a long-day pattern of melatonin each 365 days. Cycle period was 368 +/- 3 days; standard deviation of the date of onset of reproductive induction averaged only 3 days. Our study provides the first direct evidence that a single block of photoperiodic information a year can synchronize a circannual rhythm.     

Chronobiological study of several enzymes of lysosomal origin in human plasma

The possible occurrence of circadian and circannual rhythms in the plasma concentrations of the following enzymes of lysosomal origin was assessed: beta-D-N-acetylglucosaminidase (EC 3.2.1.30) beta-D-glucuronidase (EC 3.2.1.31), beta-D-glucosidase (EC 3.2.1.21), beta-D-galactosidase (EC 3.2.1.22), alpha-D-galactosidase (EC 3.2.1.23), alpha-L-fucosidase (EC 3.2.1) and alpha-D-mannosidase (EC 3.2.1.24). The circadian rhythm was studied in 16 women (aged: 17-24 years) and 13 men (age: 23 years) volunteers; the circannual rhythm, in 10 women and 8 men (age: 20-25 years). The circadian rhythm was detected in all the tested enzymes of women, and only in alpha-D-galactosidase, beta-D-glucosidase, alpha-D-mannosidase and beta-D-acetylglucosaminidase of men. A statistically significant difference between genders in the circadian rhythm was exhibited by beta-D-galactosidase (MESOR; amplitude) beta-D-glucosidase (MESOR; amplitude; acrophase) beta-D-N-acetylglucosaminidase, beta-D-glucuronidase and alpha-D-galactosidase (MESOR) and alpha-L-fucosidase (amplitude, acrophase). A circannual rhythm was detected in all the tested enzymes with the exception of beta-D-glucuronidase and beta-D-N-acetylglucosaminidase; no statistically significant difference between genders was detected. The group rhythms of some of the enzymes (alpha-D-galactosidase, beta-D-glucosidase, beta-D-galactosidase) showed similar values of both circadian and circannual acrophases, suggesting that they may subjected as a group to the same chronobiological coordination, possibly mediated by hormones. The chronobiological rhythms of lysosomal enzymes were different from those of lactate dehydrogenase and alpha 1-antitrypsin, indicating that these rhythms are not merely reflecting fluctuations of the water content of plasma. No in-phase relationship was observed between the circadian and circannual rhythms of plasma cortisol and those of the tested lysosomal enzymes, excluding a direct chronobiological and possibly functional relationship between this hormone and lysosomal enzymes.     

Circannual distribution of glioblastoma and anaplastic astrocytoma diagnoses in men and women

Background: circannual variations of incidence may influence human tumors. For example, seasonal distribution of breast cancers suggests an influence of circannual hormonal rhythms. Periodicity of brain tumors has not yet been investigated. The aim of this study was to assess the seasonal variation in glioblastomas and anaplastic astrocytomas. Methods: a large dataset of high-grade gliomas (n = 697) was evaluated with the month of diagnosis as key criterion for time series and seasonal analysis. Circannual and ultra-annual cosinor models were calculated. Results: women suffering from glioblastoma show a peak incidence in fall. No suitable circannual or ultra-annual cosinor model months could be fitted to the data. In women with anaplastic astrocytoma, a peak incidence was detected in summer and fall with a nadir in spring. Here, a significant cosinor model with a period of 8.5 months could be calculated. Conclusion: our data strongly suggest seasonality of diagnosis of high-grade gliomas in women. As gliomas express hormonal receptors, an underlying endocrinal or cell proliferation rhythms may be a possible explanation.     

Diversity of biological rhythm and food web stability

How ecosystem biodiversity is maintained remains a persistent question in the field of ecology. Here, I present a new coexistence theory, i.e. diversity of biological rhythm. Circadian, circalunar and circannual rhythms, which control short- and long-term activities, are identified as universal phenomena in organisms. Analysis of a theoretical food web with diel, monthly and annual cycles in foraging activity for each organism shows that diverse biological cycles play key roles in maintaining complex communities. Each biological rhythm does not have a strong stabilizing effect independently but enhances community persistence when combined with other rhythms. Biological rhythms also mitigate inherent destabilization tendencies caused by food web complexity. Temporal weak interactions due to hybridity of multiple activity cycles play a key role toward coexistence. Polyrhythmic changes in biological activities in response to the Earth''s rotation may be a key factor in maintaining biological communities.     

Melatonin entrainment of circannual rhythms

A melatonin-based photoperiod timing mechanism and a circannual rhythm-generating system interact to govern seasonal cycles in physiology and behavior in many vertebrates. This paper focuses on the pars tuberalis (PT) of the mammalian pituitary gland as a model melatonin-responsive tissue to investigate the molecular basis of these two basic long-term timing processes.     

Circadian and circannual rhythms of hormonal variables in elderly men and women

A group of fourteen men (73 ± 5 yr of age), and eighteen women (77 ± 7 yr of age) institutionalized at the Berceni Clinical Hospital, Bucharest, Romania, were studied over a 24-hr span once during each season (winter, spring, summer and fall). All subjects followed a diurnal activity pattern with rest at night and ate three meals per day with breakfast at about 0830, lunch at about 1300 and dinner at about 1830. The meals were similar, although not identical for all subjects during all seasons. On each day of sampling blood was collected at 4-hr intervals over a 24-hr span. Seventeen hormonal variables were determined by radioimmunoassay. Statistically significant circadian rhythms were detected and quantitated by population mean cosinor analysis in pooled data from all four seasons in both sexes for ACTH, aldosterone, Cortisol, C-peptide, dehydroepiandrosterone-sulfate (DHEA-S), immunoreactive insulin, prolactin, 17-OH progesterone, testosterone, total T₄ and TSH. In women, estradiol and progesterone also were determined and showed a circadian rhythm during all seasons. Total T, and FSH showed circadian rhythm detection by cosinor analysis in the men only; LH showed no consistent circadian rhythm as group phenomenon in men or women.

A circannual rhythm was detected using the circadian means of each subject at each season as input for the population mean cosinor in the women for ACTH, C-peptide, DHEA-S, FSH, LH, progesterone, 17-OH progesterone and TSH. In the men, a circannual rhythm was detected for ACTH, FSH, insulin, LH, testosterone and T₃. There were phase differences between men and women in ACTH, FSH and LH. In those functions in which both the circadian and circannual rhythms were statistically significant, a comparison of the amplitudes showed in the women a higher circannual rather than circadian amplitude for DHEA-S. In 17-OH progesterone, TSH and C-peptide, the circadian amplitude in women was larger. In men, the circannual amplitude of T₃ was larger than the circadian amplitude and in insulin the circadian amplitude was larger than the circannual amplitude. There was no statistically significant difference between the circadian and circannual amplitudes in the women in ACTH and progesterone and in the men in ACTH and testosterone.     

Circannual rhythms of gonadal maturation in female rainbow trout (Oncorhynchus mykiss).

Individually identified, 2-year-old female rainbow trout were maintained for up to 51 months on a constant schedule of 6 hr light and 18 hr darkness (LD 6:18), constant temperature (8.5-9.0 degrees C), and constant feeding rate. The fish exhibited free-running circannual rhythms of gonadal maturation and ovulation, which were self-sustaining for up to three cycles. The periodicity of the rhythm showed variation between fish and in successive cycles for the same fish, ranging from approximately 11 to 15 months.     

Chronobiological analysis of changes in circadian rhythm of anterior pituitary hormones level during glycemia normalization by means of biostator

We compared the circadian rhythms of anterior pituitary hormones in 15 patients with noncompensated insulin-dependent diabetes on first and second day treatment with Biostator. The rhythm was evaluated by means of a least squares analysis and presented as the circle of cosinors. In noncompensated diabetes the TSH and prolactin rhythm was maintained, whereas other hormones of the anterior pituitary showed no significant rhythm. In the course of one-day normalization of glycemia by means of Biostator the TSH and prolactin rhythm was maintained, whereas the circadian rhythm of growth hormone and ACTH levels appeared with acrophase at 18.47 and 19.59 hour, respectively. The LH rhythm did not exist, whereas the FSH rhythm was dubious. One may assume that noncompensated diabetes results in the impairment of certain pituitary hormonal rhythms and these disturbances are reversible after restoring of normoglycemia.     

From daily behavior to hormonal and neurotransmitters rhythms: Comparison between diurnal and nocturnal rat species

Mammalian species can be defined as diurnal or nocturnal, depending on the temporal niche during which they are active. Even if general activity occurs during nighttime in nocturnal rodents, there is a patchwork of general activity patterns in diurnal rodents, including frequent bimodality (so-called crepuscular pattern, i.e., dawn and dusk peaks of activity) and a switch to a nocturnal pattern under certain circumstances. This raises the question of whether crepuscular species have a bimodal or diurnal - as opposed to nocturnal - physiology. To this end, we investigated several daily behavioral, hormonal and neurochemical rhythms in the diurnal Sudanian grass rat (Arvicanthis ansorgei) and the nocturnal Long-Evans rat (Rattus norvegicus). Daily rhythms of general activity, wheel-running activity and body temperature, with or without blocked wheel, were diurnal and bimodal for A. ansorgei, and nocturnal and unimodal for Long-Evans rats. Moreover, A. ansorgei and Long-Evans rats exposed to light-dark cycles were respectively more and less active, compared to conditions of constant darkness. In contrast to other diurnal rodents, wheel availability in A. ansorgei did not switch their general activity pattern. Daily, unimodal rhythm of plasma leptin was in phase-opposition between the two rodent species. In the hippocampus, a daily, unimodal rhythm of serotonin in A. ansorgei occurred 7 h earlier than that in Long-Evans rats, whereas a daily, unimodal rhythm of dopamine was unexpectedly concomitant in both species. Multiparameter analysis demonstrates that in spite of bimodal rhythms linked with locomotor activity, A. ansorgei have a diurnally oriented physiology.     

Circadian and Circannual Rhythms of Hormonal Variables in Elderly Men and Women

A group of fourteen men (73 ± 5 yr of age), and eighteen women (77 ± 7 yr of age) institutionalized at the Berceni Clinical Hospital, Bucharest, Romania, were studied over a 24-hr span once during each season (winter, spring, summer and fall). All subjects followed a diurnal activity pattern with rest at night and ate three meals per day with breakfast at about 0830, lunch at about 1300 and dinner at about 1830. The meals were similar, although not identical for all subjects during all seasons. On each day of sampling blood was collected at 4-hr intervals over a 24-hr span. Seventeen hormonal variables were determined by radioimmunoassay. Statistically significant circadian rhythms were detected and quantitated by population mean cosinor analysis in pooled data from all four seasons in both sexes for ACTH, aldosterone, Cortisol, C-peptide, dehydroepiandrosterone-sulfate (DHEA-S), immunoreactive insulin, prolactin, 17-OH progesterone, testosterone, total T₄ and TSH. In women, estradiol and progesterone also were determined and showed a circadian rhythm during all seasons. Total T, and FSH showed circadian rhythm detection by cosinor analysis in the men only; LH showed no consistent circadian rhythm as group phenomenon in men or women.

A circannual rhythm was detected using the circadian means of each subject at each season as input for the population mean cosinor in the women for ACTH, C-peptide, DHEA-S, FSH, LH, progesterone, 17-OH progesterone and TSH. In the men, a circannual rhythm was detected for ACTH, FSH, insulin, LH, testosterone and T₃. There were phase differences between men and women in ACTH, FSH and LH. In those functions in which both the circadian and circannual rhythms were statistically significant, a comparison of the amplitudes showed in the women a higher circannual rather than circadian amplitude for DHEA-S. In 17-OH progesterone, TSH and C-peptide, the circadian amplitude in women was larger. In men, the circannual amplitude of T₃ was larger than the circadian amplitude and in insulin the circadian amplitude was larger than the circannual amplitude. There was no statistically significant difference between the circadian and circannual amplitudes in the women in ACTH and progesterone and in the men in ACTH and testosterone.     

Photic entrainment of circannual rhythms in golden-mantled ground squirrels: role of the pineal gland

Entrainment of circannual rhythms of body mass and reproduction was monitored for 3 years in female golden-mantled ground squirrels maintained in a simulated natural photoperiod. Both pinealectomized and pineal-intact squirrels generated circannual rhythms of body mass and estrus, but only the intact animals entrained these rhythms to a period of 365 days. In the second and third years after treatment, the period of the body mass rhythm was significantly shorter than 365 days for pinealectomized squirrels, and variance in tau among these animals was significantly greater than for intact squirrels. A similar pattern was evident in the rhythm of reproduction, which was phase-disrupted in pinealectomized squirrels but entrained in intacts. Seasonal changes in duration of nocturnal melatonin secretion by the pineal appear to be necessary to produce phase-delays required to entrain the circannual clock to a period of 12 months.     

麋鹿鹿角脱落、群主更替、产仔的年节律及其环境影响因子

本文在2014—2016年三个冬季(12月—翌年2月)收集了北京南海子麋鹿苑半散放麋鹿自然脱落的角,并观察和记录了2015—2017年发情期(5—9月)群主更替和2016—2018年产仔期(3—7月)麋鹿幼仔出生情况,结合2014—2018年年平均气温、季平均气温、月平均气温、年降雨量、雨季开始时间、种群密度等环境因子,对鹿角脱落、群主更替、产仔等繁殖特征的年节律及其环境影响因子进行了研究。结果表明：1)麋鹿鹿角脱落、群主更替、产仔的年节律均存在年际差异。2)鹿角脱落时间为12月开始,1月下旬或2月上旬结束。3)发情期为5月下旬或6月上旬开始,9月上旬结束;2015—2017年发情期时间有延长的趋势。4)产仔期为3月中旬或4月中旬开始,5月下旬或7月下旬结束。5)麋鹿鹿角脱落、群主更替、产仔的年节律存在明显的同步关系,其中鹿角脱落开始时间、鹿角脱落高峰期、鹿角脱落结束时间、第一次发情期开始时间、群主更替高峰期、产仔期开始时间、产仔高峰期、产仔期结束时间与前一年度比较均出现同步提前的现象。6)鹿角脱落年节律存在随着12月平均气温升高而提前的现象;产仔期开始时间和产仔高峰期存在随着前一年9月平均气温的升高而提前的现象。7)鹿角脱落年节律表现出随着年降雨量的增多而提前的现象;第一次发情期开始时间、群主更替高峰期的年节律表现出随着前一年度年降雨量的增多而提前的现象。8)麋鹿鹿角脱落、群主更替、产仔的年节律均不存在随着种群密度升高或降低而提前或延迟的现象。麋鹿繁殖特征的年节律是一个复杂的过程,受气候、营养、种群密度、纬度等环境因子的影响。     

Annual cycles of body weight in the Namie's frosted bat, Vespertilio superans superans

In order to elucidate the circannual cycles of fat deposition and depletion in hibernating bats, annual rhythm of body weight was examined in Vespertilio superans superans under a variety of environmental conditions. Under near natural conditions, adult females put on weight rapidly from October to November. The laboratory born subadult females kept in constant darkness at warm temperature gained weight at the same time as the adults. The length of weight cycle was about 10 months in adult females kept in 14 L : 10 D at about 24°C. These results suggest that cycles of fat deposition and loss are controlled by a modifiable endogenous circannual rhythm. Body weight rhythm persisted normally under warmer environmental conditions preventing the bats from hibernation. It is considered that the circannual cycles of fat gain and loss are relatively stable and not dependent on the hibernation cycle. Prolonged gestation period and delayed beginning of lactation by cold environment in summer did not affect the body weight rhythm. Temperature may be a more important environmental stimulus (or Zeitgeber) for the circannual rhythm than light and its effects may vary with phases.