Circannual Rhythm Research Articles

Research Challenges in Endocrine Aspects of Canine Ovarian Cycles

Significant deficiencies exist in understanding factors controlling the nature and timing of critical endocrine changes in canine ovarian cycles. The following merit further study: changes in steroid clearance and binding; mathematically modelling periovulatory hormone rate of change interactions; luteal gonadotropin dependence; endogenous circannual cycles underlying the ovarian cycle; importance of periovulatory follicular steroid dynamics on granulosa and oocytes; in vitro capacity of anoestrous ovarian tissue to demonstrate roles of individual gonadotropins and steroid precursors to increase oestradiol production; factors affecting secretion and activation of the canine female sex pheromone.

Preserved circannual rhythm of vitamin D in kidney transplant patients

A high prevalence of vitamin D insufficiency has been found in the general population, in patients with chronic kidney disease and in kidney transplant patients. During winter there is a higher prevalence of vitamin D insufficiency due to the lack of solar ultraviolet B (UVB) exposure. Kidney transplant patients are advised to avoid sun exposure because of their high risk of skin cancer. This is considered to be one of the main reasons for the very high prevalence of vitamin D insufficiency in these patients. Whether circannual rhythm of vitamin D is totally reversed in kidney transplant patients is not known. In this single centre prospective observational study, 50 kidney transplant patients visiting our outpatient clinic in January and February 2011 were included. Serum concentration of 25-hydroxvitamin D (25[OH]D), 1-25-hydroxvitamin D (1-25[OH]D) and intact parathormone (iPTH) were measured at study entry and 6 months later in summer. A total of 90% (45/50) of the study population had vitamin D deficiency 25(OH)D (<50 nmol/l) during winter. There was a rise of 25(OH)D in 94% (47/50) of patients from winter to summer (p <0.0001) leading to a decline of 25(OH)D deficiency from 90 to 60%, to a rise of 25(OH)D insufficiency from 6 to 26% and normal 25(OH)D from 4 to 14%, respectively (p = 0.0024). Vitamin D insufficiency during winter is very common in kidney transplant patients at our centre. Despite avoidance of exposure to UVB there is a preserved circannual rhythm of vitamin D in kidney transplant patients.

Melatonin: Circadian Regulation of Biomarkers of Oxidative Stress

Melatonin, released primarily from the pineal gland, controls the 24 hour biological clock. It is now known that melatonin also controls circannual reproductive cycles in animals and plays a role in neuroprotection, tumor-suppression, and immunomodulation. The hormone is also a potent antioxidant. This review is an attempt to document the pleiotropic biological effects of melatonin.

A tropical bird can use the equatorial change in sunrise and sunset times to synchronize its circannual clock

At higher latitudes, most organisms use the periodic changes in day length to time their annual life cycle. At the equator, changes in day length are minimal, and it is unknown which cues organisms use to synchronize their underlying circannual rhythms to environmental conditions. Here, we demonstrate that the African stonechat (Saxicola torquatus axillaris)-an equatorial songbird-can use subtle solar cues for the annual timing of postnuptial moult, a reliable marker of the circannual cycle. We compared four groups that were kept over more than 3 years: (i) a control group maintained under constant equatorial day length, (ii) a 12-month solar time group maintained under equatorial day length, but including a simulation of the annual periodic change in sunrise and sunset times (solar time), (iii) a 14-month solar time group similar to the previous group but with an extended solar time cycle and (iv) a group maintained under a European temperate photoperiod. Within all 3 years, 12-month solar time birds were significantly more synchronized than controls and 14-month solar time birds. Furthermore, the moult of 12-month solar time birds occurred during the same time of the year as that of free-living Kenyan conspecifics. Thus, our data indicate that stonechats may use the subtle periodic pattern of sunrise and sunset at the equator to synchronize their circannual clock.

Circadian and circannual rhythms of cortisol, ACTH, and α-melanocyte-stimulating hormone in healthy horses

Cosinor analysis was used to evaluate whether pituitary and adrenal hormones exhibit circadian rhythmicity in horses. The effect of season and animal age on their respective rhythms was also determined. In addition, the usefulness of evaluating cortisol rhythmicity for the diagnosis of pituitary pars intermedia dysfunction (PPID) was assessed. Serum cortisol concentrations (P < 0.01), but not plasma ACTH or α-melanocyte-stimulating hormone (α-MSH), showed a significant circadian periodicity in horses. An effect of season on hormone concentration was observed with plasma ACTH and α-MSH concentration greater in the fall and cortisol concentration greater in the spring (P < 0.001). Age did not affect cortisol rhythm, but it did blunt the variation in cortisol concentration in horses, similar to what has been previously reported to occur in aged people and dogs. In addition, our results suggest that clinically and diagnostically normal, non–PPID-affected horses commonly have a loss of cortisol diurnal rhythm. Therefore, measurement of circadian rhythm is not an appropriate diagnostic test for PPID.

Thermoregulatory changes anticipate hibernation onset by 45 days: data from free-living arctic ground squirrels

Hibernation is a strategy of reducing energy expenditure, body temperature (T(b)) and activity used by endotherms to escape unpredictable or seasonally reduced food availability. Despite extensive research on thermoregulatory adjustments during hibernation, less is known about transitions in thermoregulatory state, particularly under natural conditions. Laboratory studies on hibernating ground squirrels have demonstrated that thermoregulatory adjustments may occur over short intervals when animals undergo several brief, preliminary torpor bouts prior to entering multiday torpor. These short torpor bouts have been suggested to reflect a resetting of hypothalamic regions that control T(b) or to precondition animals before they undergo deep, multiday torpor. Here, we examined continuous records of T(b) in 240 arctic ground squirrels (Urocitellus parryii) prior to hibernation in the wild and in captivity. In free-living squirrels, T(b) began to decline 45 days prior to hibernation, and average T(b) had decreased 4.28 °C at the onset of torpor. Further, we found that 75 % of free-living squirrels and 35 % of captive squirrels entered bouts of multiday torpor with a single T(b) decline and without previously showing short preliminary bouts. This study provides evidence that adjustments in the thermoregulatory component of hibernation begin far earlier than previously demonstrated. The gradual reduction in T(b) is likely a component of the suite of metabolic and behavioral adjustments, controlled by an endogenous, circannual rhythm, that vary seasonally in hibernating ground squirrels.

Uric acid biorhythm, a feature of long-term variation in a clinical laboratory database

The biorhythm of serum uric acid was evaluated in a large sample of a clinical laboratory database by spectral analysis and the influence of the gender and age on uric acid variability. Serum uric acid values were extracted from a large database of a clinical laboratory from May 2000 to August 2006. Outlier values were excluded from the analysis and the remaining data (n=73,925) were grouped by gender and age ranges. Rhythm components were obtained by the Lomb Scargle method and Cosinor analysis. Serum uric acid was higher in men than in women older than 13 years (p<0.05). Compared with 0-12 year group, uric acid increased in men but not in women older than 13 years (p<0.05). Circannual (12 months) and transyear (17 months) rhythm components were detected, but they were significant only in adult individuals (>26 years, p<0.05). Cosinor analysis showed that midline estimating statistic of rhythm (MESOR) values were higher in men (range: 353-368 μmol/L) than in women (range: 240-278 μmol/L; p<0.05), independent of the age and rhythm component. The extent of predictable change within a cycle, approximated by the double amplitude, represented up to 20% of the corresponding MESOR. Serum uric acid biorhythm is dependent on gender and age and it may have relevant influence on preanalytical variability of clinical laboratory results.

Physiological and behavioral responses of migrants to environmental cues

Migrant species express wide varieties of movement strategies that closely mirror patterns of resource distribution. Resources can vary predictably in space and time (e.g., seasonal peaks of productivity in temperate regions) or can be unpredictable in one or both dimensions. Evolution of migration strategies and the underlying physiological and behavioral mechanisms are therefore diverse, but similarities have been noted. To understand how migrants respond to environmental cues, we focus on species that represent extremes along a continuum between obligate versus facultative migratory behavior and address the physiological mechanisms regulating these movements. Obligate migrants, which travel on highly predictable schedules, generally rely on the annual change in daylength and circannual rhythms to initiate the vernal and, where known, the fall phases of migration. Facultative species may show similar seasonal preparations in cases where resources are temporally predictable, but appear to rely more heavily upon local supplementary cues in the environment to initiate migrations. In general, the physiological response mechanisms to environmental cues that coordinate migratory movements include perception of the environmental cue and transduction to neuroendocrine and endocrine systems. Clearly, there are huge gaps in our knowledge in this area, but published studies of each of the migratory types suggest striking parallels. Based on a comparison of the physiological aspects of the divergent migratory patterns, we emphasize that the migratory types are not completely distinct. Instead, the differences of migration patterns and responsiveness to cues reflect differences in the relative contributions of common physiological mechanisms that underly the control of movements. A more complete understanding of migratory physiology requires continued descriptive studies, particularly in a greater diversity of model systems, in addition to experimental methods that utilize innovative tracking technology as well as behavioral and physiological innovations to draw attention to different levels of organization. Comprehending the physiological mechanisms underlying migratory patterns will be vital for knowing how migrants respond to current environmental cues and anticipating their reactions to future conditions.

Effect of TiO2 nanoparticles in the earthworm reproduction test

Abstract Background The increasing use of nanotechnology means that nanomaterials will enter the environment. Ecotoxicological data are therefore required so that adequate risk assessments can be carried out. In this study, we used a standardized earthworm reproduction test with Eisenia andrei to evaluate three types of TiO2 nanoparticles (NM-101, NM-102, NM-103). The test was performed in natural sandy soil (RefeSol 01A) following Organisation for Economic Co-operation and Development Test Guideline No. 222. The nanoparticles differed in several aspects, such as crystalline structure, size, and the presence or absence of a coating. Results Uncoated nanoparticles stimulated earthworm reproduction in a concentration-dependent manner during winter testing, increasing the number of offspring by up to 50% compared to the control. However, there was no stimulation when the same test was performed in the summer. This reflected an underlying circannual rhythm observed in the control soil, characterized by the production of a significantly larger number of juveniles in summer compared with that in winter. The effect of the uncoated TiO2 nanoparticles was to reduce or eliminate the circannual differences by increasing the reproductive rate in winter. Coated TiO2 nanoparticles did not influence earthworm reproduction. Conclusion TiO2 appears to affect earthworm reproductive activity by abolishing the circannual rhythm that depresses reproduction in the winter. Further experiments will be necessary to determine (1) the mode of action of the nanoparticles, (2) the important parameters causing the effect (e.g., relevant soil parameters), and (3) the environmental relevance of continuous earthworm reproduction we observed under laboratory conditions.

Persistence of circannual rhythms under constant periodic and aperiodic light conditions: sex differences and relationship with the external environment

The timing and duration of gonadal phases in the year indicates that breeding cycles are regulated by endogenous mechanisms. The present study on tropical spotted munia (Lonchura punctulata) investigates whether such mechanisms are based on circannual rhythms, and whether circannual rhythms between sexes differ in their relationship with the light environment. Birds were subjected to 12 h light per day (12L:12D), alternate days of light and darkness (24L:24D, LL/DD) and continuous light (LL), with L=22 lx and D≤1 lx, for 28 months at constant temperature (18±1°C). Groups kept on natural day lengths (NDL) served as controls. Measurement of body mass, gonads and molts of the primary wing feathers and body plumage at regular intervals showed that birds underwent repeated cycles in gonads and molt, but not in body mass. Under NDL, gonadal phases in both sexes cycled with 12 month periods. Under other conditions, males cycled with similar periods of ~11 months, but females cycled with relatively large period variations, ~10-13 months. Gonadal recrudescence-regression phase was longer in males than in females and, in both sexes, longer in the second year compared with the first year. The molt of wing primaries was more closely coupled to gonadal maturation in groups on NDL and 12L:12D than in groups on LL and LL/DD, but this relationship drifted apart in the second year. Body plumage molts were relatively more highly variable in both frequency and pattern in females than in males. It is suggested that annual breeding cycle in spotted munia is regulated by the self-sustained circannual rhythms, which probably interact with the annual photoperiodic cycle to synchronize breeding cycles to calendar year. Both sexes seem to have independent timing strategies, but females appear to share a greater role in defining the reproductive season in relation with the environment.

The thymus and adaptive changes in the cellular composition of bone marrow in animals of different ages

This article studies the influence of the removal of the thymus or the administration of its biologically active factor (Thymalin) on a number of stromal precursor cells for colonies of fibroblasts (CFC-F cells), progenitor cells for granulocyte-macrophage colonies (CFC-GM cells), and CD4+ cells in bone marrow in CBA mice of different ages in different seasons of the year. It is established that in adult mice, changes of the thymus function by the number of these cell types depend on the season. This shows the possibility of a direct effect of a thymic stroma supernatant containing thymic serum factor (FTS) and synthetic FTS on the number of CFC-F and CFC-GM cells in the bone marrow of adult mice in different seasons; in old animals thymic supernatant increased the number of CD4+ cells in vitro. Administration of Thymalin to old mice led to an increase of the titer of FTS in the blood, the restoration of disturbed circannual rhythm, the number of CD4+ cells in the bone marrow, and the concentration of corticosterone in the blood.

Hypothesis

Circannual rhythms are innately timed long-term (tau ≈ 12 months) cycles of physiology and behavior, crucial for life in habitats ranging from the equator to the Poles. Here the authors propose that circannual rhythm generation depends on tissue-autonomous, reiterated cycles of cell division, functional differentiation, and cell death. They see the feedback control influencing localized stem cell niches as crucial to this cyclical histogenesis hypothesis. Analogous to multi-oscillator circadian organization, circannual rhythm generation occurs in multiple tissues with hypothalamic and pituitary sites serving as central pacemakers. Signals including day length, nutrition, and social factors can synchronize circannual rhythms through hormonal influences, notably via the thyroid and glucocorticoid axes, which have profound effects on histogenesis. The authors offer 4 arguments in support of this hypothesis: (1) Cyclical histogenesis is a prevalent process in seasonal remodeling of physiology. It operates over long time domains and exhibits tissue autonomy in its regulation. (2) Experiments in which selected peripheral endocrine signals are held constant indicate that circannual rhythms are not primarily the product of interacting hormonal feedback loops. (3) Hormones known to control cell proliferation, differentiation, and organogenesis profoundly affect circannual rhythm expression. (4) The convergence point between photoperiodic input pathways and circannual rhythm expression occurs in histogenic regions of the hypothalamus and pituitary. In this review, the authors discuss how testing this hypothesis will depend on the use of cellular/molecular tools and animal models borrowed from developmental biology and neural stem cell research.

The regulation of food intake in mammalian hibernators: a review

One of the most profound hallmarks of mammalian hibernation is the dramatic reduction in food intake during the winter months. Several species of hibernator completely cease food intake (aphagia) for nearly 7months regardless of ambient temperature and in many cases, whether or not food is available to them. Food intake regulation has been studied in mammals that hibernate for over 50years and still little is known about the physiological mechanisms that control this important behavior in hibernators. It is well known from lesion experiments in non-hibernators that the hypothalamus is the main brain region controlling food intake and therefore body mass. In hibernators, the regulation of food intake and body mass is presumably governed by a circannual rhythm since there is a clear seasonal rhythm to food intake: animals increase food intake in the summer and early autumn, food intake declines in autumn and actually ceases in winter in many species, and resumes again in spring as food becomes available in the environment. Changes in circulating hormones (e.g., leptin, insulin, and ghrelin), nutrients (glucose, and free fatty acids), and cellular enzymes such as AMP-activated protein kinase (AMPK) have been shown to determine the activity of neurons involved in the food intake pathway. Thus, it appears likely that the food intake pathway is controlled by a variety of inputs, but is also acted upon by upstream regulators that are presumably rhythmic in nature. Current research examining the molecular mechanisms and integration of environmental signals (e.g., temperature and light) with these molecular mechanisms will hopefully shed light on how animals can turn off food intake and survive without eating for months on end.

CATALYTIC RECEPTORS

CATALYTIC RECEPTORS

Kisspeptin Cells in the Ovine Arcuate Nucleus Express Prolactin Receptor but not Melatonin Receptor

Melatonin is secreted at night by the pineal gland and governs the reproductive system in seasonal breeders, such as sheep. The mechanism by which melatonin regulates reproduction is not known. The circannual rhythmicity of other factors, including prolactin, is also regulated by photoperiod via changes in melatonin secretion. In sheep, plasma prolactin levels are higher in the nonbreeding season than the breeding season. Kisspeptin, synthesised by neurones in the ovine arcuate nucleus (ARC) and preoptic area, is a key regulator of reproduction through stimulation of gonadotrophin-releasing hormone secretion and its expression in the ARC is reduced during the nonbreeding season. We hypothesised that kisspeptin expression is directly, or indirectly, regulated by melatonin and/or prolactin. We first examined the expression of melatonin receptor (MTNR1A) in kisspeptin (Kiss1 mRNA) neurones in the ARC of ovariectomised (OVX) sheep using double-label in situ hybridisation. MTNR1A mRNA was not expressed by kisspeptin neurones, whereas strong expression was detected in the pars tuberalis. We then examined the expression of the long-form prolactin receptor (PRLR-L) in ARC kisspeptin neurones. In OVX ewes, approximately 60% of kisspeptin neurones expressed PRLR-L mRNA at similar levels in the breeding and nonbreeding seasons. We then aimed to determine whether prolactin treatment during the breeding season regulates kisspeptin expression in the ARC. Continuous central infusion of prolactin (20 μg/h for 7 days) in oestradiol-treated OVX sheep did not alter Kiss1 mRNA expression or luteinising hormone secretion, although it induced substantial phosphorylated signal transducer and activator of transcription 5-immunoreactive nuclei staining in the mediobasal hypothalamus. We conclude that the seasonal change in kisspeptin neurones cannot be regulated directly by melatonin, although it may be a result of changes in prolactin levels. Despite this, kisspeptin expression was unchanged after exogenous prolactin treatment in breeding season ewes.

Circadian and circannual rhythms in RA

Early symptoms of arthritis either resolve spontaneously or progress into erosive disease; being able to predict the disease course would inform decisions about intensive early therapy. One predictive factor, according to a new multicenter study, is the season of first symptoms—so how does the Earth's movement influence disease progression?

Seasonal variation of long-term potentiation at a central synapse in the medicinal leech

Long-term potentiation (LTP) is a persistent increase in synaptic transmission that is thought to contribute to a variety of adaptive processes including learning and memory. Although learning is known to undergo circannual variations, it is not known whether LTP undergoes similar changes despite the importance of LTP in learning and memory. Here we report that synapses in the CNS of the medicinal leech demonstrate seasonal variation in the capacity to undergo LTP following paired presynaptic and postsynaptic stimulation. LTP was observed during the April-October period, but no LTP was observed during the November-March period. Application of forskolin, a technique often used to produce chemical LTP, failed to elicit potentiation during the November-March period. Implementing stimulation patterns that normally result in long term depression (LTD) also failed to elicit any change in synaptic strength during the November-March period. These experiments indicate that LTP and LTD can be influenced by circannual rhythms and also suggest a seasonal influence on learning and memory.

What drives seasonal fluctuations of body condition in a semelparous income breeder octopus?

The vast majority of modern cephalopods is single-season breeders, or semelparous in the strict sense, that die soon after the reproduction takes place. Individual body condition in these marine invertebrates is expected to be highly affected by reproduction because: 1) the gonad weight of females, which represents <1% of body weight when immature, increases up to 20–50% during maturation; and 2) octopus females reduce or even cease their food intake during breeding. Based on this expectation, we analysed the interrelationship between condition and reproduction in the temperate octopus Eledone cirrhosa. Results from a previous work using biochemical analyses showed that reproduction in this species is not fuelled by stored reserves (capital breeder), but by food intakes (income breeder). Since income breeders depend strongly on food resources, the effect of several environmental variables related to food availability such as primary production, sea temperature (ST) and river discharges were also analysed. Condition showed a marked intrannual cycle independently of the sex and, noteworthy, the maturity stage. Given that immature individuals are not expected to display seasonal fluctuations in body condition related to maturation, these results preclude reproduction as a driving factor for the observed circannual cycle. Condition was significantly correlated with all the environmental variables analysed, except with ST at the depths where the species lives. Although this last result also precludes concurrent ST as a driving factor of body condition, those correlations suggest that condition might display an intrinsic seasonal cycle, as many other life-history traits in most species such as reproduction, migration or moulting. Finally, there also remains the possibility that condition in this octopus species is determined genetically, as has been reported in recent studies across different taxonomical groups.

Review: feed withdrawal and non feed withdrawal moult

Moulting is a natural phenomenon in birds. Temperature variation and photoperiodic changes induce circadian and circannual rhythms, manifested by changes in the neural and endocrine systems, ultimately causing physiological processes resulting in a moult. The concept of induced moulting by feed deprivation arose during the early part of the 20th century as a solution to economic challenges of decreased egg production in commercial layer flocks toward the end of the first laying cycle as they approached the moult phase. Efficiency of feed removal programs in enhancing post moult productivity and economical feasibility insured a gain in popularity by the 1930′s. In 2003, more than 75% of all flocks were moulted in the U.S. However, moulting with feed withdrawal caused risk to the health of birds by impairing the immune system and increasing susceptibility to various pathogens, especially Salmonella enteritidis (SE). During the 1980s, increased incidence of gastroenteritis due to SE was linked to forced moulting. The importance of challenges for conventional forced moulting was realized and animal activists, welfare organizations, researchers, consumers, and producers realized that alternative moulting methods were necessary. Ultimately, the United Egg Producers Scientific Advisory Committee, having dealt with the issue of feed withdrawal for moulting since the early 1990′s, amended the Animal Husbandry Guidelines for U.S. Egg Laying Flocks to specify the use of non feed withdrawal moult methods after January 1, 2006. Furthermore, moulting hens would have to be fed nutritionally adequate and palatable food suitable for non-egg producing hens. Though metals or hormones are efficient moult inducers, results of studies showed that they had disadvantages like residual effects and physiological alterations, respectively. Diets supplemented with low nutritious feed ingredients are safe and demonstrate promising outcomes. Unconventional feedstuffs such as coconut meal and cumin seed meal are successfully used in layer and non feed removal moults in Asian and Middle Eastern countries. In the western U.S. (especially in California), local ingredients like safflower meal and tomato pomace are promising alternatives.

Diet-Independent Remodeling of Cellular Membranes Precedes Seasonally Changing Body Temperature in a Hibernator

Polyunsaturated fatty acids (PUFA) have a multitude of health effects. Their incorporation into membrane phospholipids (PL) is generally believed to depend directly on dietary influx. PL influence transmembrane protein activity and thus can compensate temperature effects; e.g. PL n-6 PUFA are thought to stabilize heart function at low body temperature (Tb), whereas long chain (>C18) n-3 PUFA may boost oxidative capacity. We found substantial remodeling of membranes in free-living alpine marmots which was largely independent of direct dietary supply. Organ PL n-6 PUFA and n-6 to n-3 ratios were highest at onset and end of hibernation after rapid increases during a brief transitional period prior to hibernation. In contrast, longer chain PL n-3 PUFA content was low at end of summer but maximal at end of hibernation. After termination of hibernation in spring, these changes in PL composition were rapidly reversed. Our results demonstrate selective trafficking of PUFA within the body, probably governed by a circannual endogenous rhythm, as hibernating marmots were in winter burrows isolated for seven months from food and external cues signaling the approaching spring. High concentrations of PL n-6 PUFA throughout hibernation are in line with their hypothesized function of boosting SERCA 2a activity at low Tb. Furthermore, we found increasing rate of rewarming from torpor during winter indicating increasing oxidative capacity that could be explained by the accumulation of long-chain PL n-3 PUFA. It may serve to minimize the time necessary for rewarming despite the increasing temperature range to be covered, because rewarming is a period of highest metabolic rate and hence production of reactive oxygen species. Considering the importance of PUFA for health our results may have important biomedical implications, as seasonal changes of Tb and associated remodeling of membranes are not restricted to hibernators but presumably common among endothermic organisms.