Synchronization of circannual cycles: a cold spring delays the cycles of thirteen-lined ground squirrels

Summary Ground squirrels, show circannual cycles with periods normally less than a year when kept under laboratory conditions. The way in which environmental factors synchronize these cycles with the geophysical year under natural conditions is not known. We tested the possibility that cold temperatures can cause long-term phase delays in circannual cycles of thirteen-lined ground squirrels.Two groups of animals were kept in the cold (4 °C) for either 8.5 or 13 months, after which they were returned to the warm (21 °C) and kept there until they had completed at least one additional cycle. A third group was kept in the warm for the entire experiment. Most of the males in the cold room groups became arrested in the spring phase of their cycles while they were in cold. When returned to the warm, these males resumed cycling. When animals showed prolonged spring phases, their cycles were phase-delayed and continued to reflect this delay even after they were returned to the warm. Both body weight cycles and molt cycles were delayed. In contrast to the males in the cold room, none of the females in the cold room groups and none of the warm room animals of either sex showed this response.Our results demonstrate that cold temperatures can phase-delay both body weight and molt cycles and that the spring phase is a critical stage in this effect. We suggest that spring temperatures are largely responsible for the seasonal synchronization of circannual cycles in ground squirrels and are, therefore, a possible Zeitgeber for these cycles.     

Circannual control of hibernation by HP complex in the brain

Seasonal hibernation in mammals is under a unique adaptation system that protects organisms from various harmful events, such as lowering of body temperature (Tb), during hibernation. However, the precise factors controlling hibernation remain unknown. We have previously demonstrated a decrease in hibernation-specific protein (HP) complex in the blood of chipmunks during hibernation. Here, HP is identified as a candidate hormone for hibernation. In chipmunks kept in constant cold and darkness, HP is regulated by an individual free-running circannual rhythm that correlates with hibernation. The level of HP complex in the brain increases coincident with the onset of hibernation. Such HP regulation proceeds independently of Tb changes in constant warmth, and Tb decreases only when brain HP is increased in the cold. Blocking brain HP activity using an antibody decreases the duration of hibernation. We suggest that HP, a target of endogenously generated circannual rhythm, carries hormonal signals essential for hibernation to the brain.     

Hibernation does not affect memory retention in bats

Long-term memory can be critically important for animals in a variety of contexts, and yet the extreme reduction in body temperature in hibernating animals alters neurochemistry and may therefore impair brain function. Behavioural studies on memory impairment associated with hibernation have been almost exclusively conducted on ground squirrels (Rodentia) and provide conflicting results, including clear evidence for memory loss. Here, we for the first time tested memory retention after hibernation for a vertebrate outside rodents—bats (Chiroptera). In the light of the high mobility, ecology and long life of bats, we hypothesized that maintenance of consolidated memory through hibernation is under strong natural selection. We trained bats to find food in one out of three maze arms. After training, the pre-hibernation performance of all individuals was at 100 per cent correct decisions. After this pre-test, one group of bats was kept, with two interruptions, at 7°C for two months, while the other group was kept under conditions that prevented them from going into hibernation. The hibernated bats performed at the same high level as before hibernation and as the non-hibernated controls. Our data suggest that bats benefit from an as yet unknown neuroprotective mechanism to prevent memory loss in the cold brain.     

Extensive use of torpor in 13-lined ground squirrels in the fall prior to cold exposure

Mammalian hibernation is characterized by profound reductions in body temperature (T _b) and metabolic, heart and respiratory rates. These reductions are characteristic of torpor, which is temporally confined to winter. Hibernators including ground squirrels are heterothermic in winter, cycling between multiday periods of torpor with low T _b and brief periods of rewarming. In contrast, ground squirrels remain homeothermic during summer, like non-hibernating mammals. The transition between the homeothermic and heterothermic phases of the circannual rhythm of hibernation is often overlooked in hibernation studies. Here, we examined the use of torpor throughout the fall transition in laboratory-housed 13-lined ground squirrels by recording core body temperature with an implanted data logger. As is typical of laboratory-based hibernation studies, animals were kept in standard housing prior to being moved into a cold, dark room to simulate natural hibernation conditions. Significantly, the vast majority of both male and female ground squirrels expressed torpor in the fall while still housed conventionally and prior to cold exposure. The expression of torpor was not predicted by body weight or age, rather it appears to be preprogrammed in a time-dependent manner that is independent of, yet enhanced by, environmental cues. The timing and duration of these torpor bouts occurring prior to cold exposure were also remarkably sporadic. Thus, it is not possible to know with certainty which animals are torpor-naive before cold exposure in the absence of continuous measurement of body temperature. We conclude that fall animals encompass variable points in the transition between summer and winter phases of the circannual cycle of hibernation, thereby confounding studies in which they are used as non-hibernating controls. Conversely, these fall transition animals offer unique opportunities to define the molecular changes that accompany and enable hibernation.     

Circannual cycles in golden-mantled ground squirrels: Experiments with food deprivation and effects of temperature on periodicity

Summary Female golden-mantled ground squirrels,Spermophilus lateralis, kept in a cool room (9.5 °C), were food deprived and their hibernation thereby extended by 11 weeks on average compared to undeprived control animals in the same room. The deprived group was then refed. Despite their prolonged hibernation, peak weights and onset of hibernation in the subsequent season were only 2–4 weeks later than in the undeprived controls and this effect was only marginally significant. However, the periods of circannual cycles of both the deprived and undeprived groups in the cool room were significantly longer than those of another group of female ground squirrels kept in a warm room (21 °C). It is argued that warm temperatures are capable of terminating the winter phase of circannual cycles, namely that of hibernation and declining body weight. If animals are kept continuously in a cool environment this phase ends spontaneously. Even many weeks of food deprivation are only capable of extending this phase by a relatively small amount, if at all.The author thanks Kirsteen Lang for invaluable help at every phase of this work, Linda Jones and others at the Environmental Sciences Centre, Kananaskis, for heir cooperation, and Janice Farintosh, John Ting and Yasmin Shah for collecting data. Support came from the Natural Sciences and Engineering Research Council of Canada.     

Changes in body condition of hibernating bats support the thrifty female hypothesis and predict consequences for populations with white-nose syndrome

White-nose syndrome (WNS) is a new disease of bats that has devastated populations in eastern North America. Infection with the fungus, Geomyces destructans, is thought to increase the time bats spend out of torpor during hibernation, leading to starvation. Little is known about hibernation in healthy, free-ranging bats and more data are needed to help predict consequences of WNS. Trade-offs presumably exist between the energetic benefits and physiological/ecological costs of torpor, leading to the prediction that the relative importance of spring energy reserves should affect an individual''s use of torpor and depletion of energy reserves during winter. Myotis lucifugus mate during fall and winter but females do not become pregnant until after spring emergence. Thus, female reproductive success depends on spring fat reserves while male reproductive success does not. Consequently, females should be “thrifty” in their use of fat compared to males. We measured body condition index (BCI; mass/forearm length) of 432 M. lucifugus in Manitoba, Canada during the winter of 2009/2010. Bats were captured during the fall mating period (n = 200), early hibernation (n = 125), and late hibernation (n = 128). Adult females entered hibernation with greater fat reserves and consumed those reserves more slowly than adult males and young of the year. Consequently, adult females may be more likely than males or young of the year to survive the disruption of energy balance associated with WNS, although surviving females may not have sufficient reserves to support reproduction.     

Energy balance of hibernating mouse-eared batMyotis myotis: a study with a TOBEC instrument

We used a non-invasive TOBEC method (Total Body Electric Conductivity) to estimate lean body mass and fat content in mouse-eared batsMyotis myotis (Borkhausen, 1797) hibernating in Poznañ Forts (W Poland) and in a semi-natural cave-mine Miedzianka (SE Poland). In December, fat content averaged 5.5 g in females (body mass = 29.4 g) and 5.3 g in males (body mass = 28.4 g). At the end of hibernation (April), fat content averaged 2.2 g in females (body mass = 25.6 g) and 1.4 g in males (body mass = 23.7 g). Fat content did not differ between the localities either in December or in April, but the pattern of changes of fat content was different. We calculated the rate of energy expenditure in hibernating bats using two methods, based on independent samples (fat content in first-time captured individuals) and based on paired observations (changes of fat content in re-captured individuals), and discussed problems associated with the two approaches. Both methods show that the bats need about 4.9 g of fat (191 kJ) to sustain a 165-day hibernation. However, the rate of fat usage varied considerably between the sites and hibernation phase. Although the average amount of fat remaining in April would be sufficient to support at least six more weeks of hibernation, the level of reserves was close to zero in some individuals.     

Further demonstration of the ambient temperature dependence of the annual biological cycles in the edible dormouse,Glis glis

Summary In the male edible dormouse, it has been proposed that the annual temperature cycle is the major external factor triggering annual biological rhythms in this hibernating species. The present study was designed to explore (i) the effects of suppression of the annual thermoperiodic cycle under natural photoperiodic conditions, and (ii) the effects of acute exposure to a warm environment on basal plasma T4 levels observed during hibernation. The results of the first experiment demonstrate an absence of circannual cycles of hibernation, body weight, and endocrine thyroid and gonadal functions in the absence of annual fluctuations of temperature (constant warm environment at 24°C) despite the maintenance of a normal photoperiodic cycle. On the other hand, acute exposure to 24°C during the late stage of hibernation stimulated thyroid function as expressed by a consistent transitory rise in plasma T4 concentrations, which was maximal within 7 days and restored to basal levels after 14 days. These findings are in close agreement with the concept that in the edible dormouse, the annual thyroid cycle is synchronized with the annual temperature cycle. Moreover, the present study, combined with prior data indicating that the thyroid cycle induces the testis cycle, suggests that the ambient temperature cycle may be intricately involved in the control of neuroendocrine cycles in dormice, although the mechanism is still unknown.     

Hibernation in garter snakes (Thamnophis sirtalis parietalis): seasonal cycles of cold tolerance

1. The red-sided garter snake hibernates for about six months each year in Manitoba, Canada, where winter temperatures are often as low as -40 degrees C. Mammalian hibernators typically undergo profound changes in preparation for hibernation, but little is known about corresponding changes in reptiles. 2. We tested the importance of seasonal changes in the ability of red-sided garter snakes to hibernate successfully by exposing them to winter conditions at different times of year. 3. Animals that began hibernation in the fall were more likely to survive hibernation than animals that began hibernation in either early or late summer, despite the fact that the animals were kept on seasonally constant conditions prior to hibernation. 4. We suggest that these changes are derived from endogenous components of the yearly hibernation cycle of red-sided garter snakes but that only part of the cycle proceeds endogenously, i.e. it is not a completely endogenous circannual cycle.     

Factor affecting body mass of young fat dormics (Glis glis) at weaning and by hibernation

This paper describes the factors affecting body mass at weaning and by hibernation of young fat dormice (Glis glis) We studied a free-living population in 1991 and 1992 in a mixed forest where 100 nest-boxes were placed. In the two years, 128 females used the nest-boxes to give birth and rear their litters and more than 900 dormice have been individually marked. Body mass of young at weaning was positively correlated to body mass of the mother in both years and to birth date in 1991, while litter size was negatively correlated to body mass of the young in 1992 only, when birth took place about two weeks later than in 1991. On the contrary, by the time of hibernation, young born later weighed significantly less than those born earlier in the season, and heavier young at weaning remained heavier by hibernation, while maternal body mass and litter size did not significantly affect body mass of young at this stage. Body mass of the mother was negatively related to the date of parturition and early breeding females lost weight during lactation, while females that bred later did not. It seems, therefore, that early breeding carries a cost that only females in good condition can afford. It appears that females may follow two strategies: those in poor body condition will delay pregnancy so that lactation occurs when environmental feeding conditions are at their best; those in good condition will breed earlier, since they can afford to lose weight during lactation. Their young will have more time to grow before hibernation and the mothers themselves will have a longer period of time for restoring their fat reserves.     

Circannual Growth Rhythm in a Brown Alga,Pterygophora californica

A circannual rhythm was found in the kelp Pterygophora californica which forms a new blade with a free running period of 7 ? 8 months under constant conditions. Individual plants exposed to cycles of daylength with T = 12, 6, or 3 months performed 1, 2, or 4 growth cycles, respectively, in one calendar year showing the entrainment of the endogenous circannual rhythm. The annual growth cycle also followed a phase shift of the annual cycle of daylength (T = 12 months) by 3 or 6 months.     

Non-gonadal mediated effect of photoperiod on hibernation and body weight cycles of the European hamster

1. Sexually active male European hamsters raised under short photoperiod display high levels of plasma testosterone, high body weight and do not hibernate. 2. Castrated males in May, raised under the same conditions, do not hibernate and do not present the physiological body weight rhythm. 3. Normal and castrated animals under natural conditions enter hibernation and display a normal body weight rhythm. 4. Normal and castrated animals not submitted to the natural succession of long and short days do not enter hibernation. 5. Photoperiod directly controls body weight and hibernation gonadal interactions.     

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.     

季节、环境温度与黄鼠冬眠的关系

观察了达乌尔黄鼠在实验室内冬眠的一般情况。常温黄鼠的体温有着规律性的年周期,与环境温度的年周期变动不完全呈依从关系。出眠初期(4月下旬),动物体温高而稳定。4月至6月常温黄鼠的平均体温(皮温)为35.6℃,波动菹围32—37.5℃。随着体重达到顶峰,体温逐渐降低。8月份部分黄鼠出现低于32℃的低常体温,表明部分黄鼠自8月盛夏开始冬眠。但就整个种群而言,北京地区实验室内黄鼠冬眠季自9月下半月开始。3月底止,共6.5个月。秋季室温下降,动物入眠趋势增长。浅低体温(31.9—15℃)的比数逐渐升高。9月至12月,低体温(低于31.9℃)的百分比从47％增至84.8％,反映了动物从浅冬眠向深冬眠过渡。1月至2月份,低体温占85％以上,深低体温(低于15℃)占绝对优势。标志着动物种群的深眠月份。秋季动物从常温期向冬眠期转化的界线是不清的,而春季从冬眠期向常温相转化的界限却比较明显。     

Avian circannual clocks: adaptive significance and possible involvement of energy turnover in their proximate control

Endogenous circannual clocks are found in many long-lived organisms, but are best studied in mammal and bird species. Circannual clocks are synchronized with the environment by changes in photoperiod, light intensity and possibly temperature and seasonal rainfall patterns. Annual timing mechanisms are presumed to have important ultimate functions in seasonally regulating reproduction, moult, hibernation, migration, body weight and fat deposition/stores. Birds that live in habitats where environmental cues such as photoperiod are poor predictors of seasons (e.g. equatorial residents, migrants to equatorial/tropical latitudes) rely more on their endogenous clocks than birds living in environments that show a tight correlation between photoperiod and seasonal events. Such population-specific/interspecific variation in reliance on endogenous clocks may indicate that annual timing mechanisms are adaptive. However, despite the apparent adaptive importance of circannual clocks, (i) what specific adaptive value they have in the wild and (ii) how they function are still largely untested. Whereas circadian clocks are hypothesized to be generated by molecular feedback loops, it has been suggested that circannual clocks are either based upon (i) a de-multiplication ('counting') of circadian days, (ii) a sequence of interdependent physiological states, or (iii) one or more endogenous oscillators, similar to circadian rhythms. We tested the de-multiplication of days (i) versus endogenous regulation hypotheses (ii) and (iii) in captive male and female house sparrows (Passer domesticus). We assessed the period of reproductive (testicular and follicular) cycles in four groups of birds kept either under photoperiods of LD 12L:12D (period length: 24h), 13.5L:13.5D (27 h), 10.5L:10.5D (23 h) or 12D:8L:3D:1L (24-h skeleton photoperiod), respectively, for 15 months. Contrary to predictions from the de-multiplication hypothesis, individuals experiencing 27-h days did not differ (i.e. did not have longer) annual reproductive rhythms than individuals from the 21- or 24-h day groups. However, in line with predictions from endogenous regulation, birds in the skeleton group had significantly longer circannual period lengths than all other groups. Birds exposed to skeleton photoperiods experienced fewer light hours per year than all other groups (3285 versus 4380) and had a lower daily energy expenditure, as tested during one point of the annual cycle using respirometry. Although our results are tantalizing, they are still preliminary as birds were only studied over a period of 15 months. Nevertheless, the present data fail to support a 'counting of circadian days' and instead support hypotheses proposing whole-organism processes as the mechanistic basis for circannual rhythms. We propose a novel energy turnover hypothesis which predicts a dependence of the speed of the circannual clock on the overall energy expenditure of an organism.     

Persistence of a circannual rhythm of plasma prolactin concentrations in ewes exposed to a constant equatorial photoperiod

Circulating concentrations of prolactin were monitored for 3 yr in intact ewes kept either outdoors or indoors in a fixed equatorial photoperiod (12L:12D) and restricted range of environmental temperatures. Prolactin data were analyzed by spectral analysis. In all ewes kept outdoors, concentrations of prolactin showed robust circannual rhythms with a single predominant period of 359 days. In ewes kept indoors, the range of significant periods varied from 35 to 532 days. Although all ewes kept indoors showed a significant rhythm with a period of 354 days, this clearly was not the predominant period in all. The amplitude of the rhythm in ewes kept indoors was significantly lower (p less than 0.01) than that of ewes kept outdoors. Although the annual rhythm of circulating prolactin typical of ewes kept outdoors was significantly compromised in animals kept under a constant 12L:12D photoperiod and restricted environmental temperature range, there was evidence of an endogenous circannual rhythm.     

Effect of pinealectomy on free-running reproductive cycle of tropical spotted munia

Summary The breeding cycle of the tropical spotted munia (Lonchura punctulata) is regulated by the photoperiodic synchronization of an endogenous circannual rhythm. Since the pineal gland has been implicated in circadian periodicity, in an attempt to understand the functioning of the mechanism(s) involved in photoperiodic synchronization of the circannual clock in the spotted munia the effect of pinealectomy on the reproductive cycle was studied in birds maintained in normal entrained (natural day length, NDL) and free-running (constant light, LL) conditions.Results indicate that pinealectomy had no effect in LL but that the reproductive cycle was altered marginally (in the first cycle only), and the body weight cycle drastically, in NDL conditions. It seems that the marginal effects observed on the overt reproductive cycle in the entrained condition may not be through the circannual oscillator itself but may perhaps reflect interference with processes involved in photoperiodic synchronization of the circannual rhythm. Alternatively, these effects could also result from general metabolic disturbances caused in the body by the absence of the pineal gland.Abbreviations LL constant light - NDL natural day length     

Investigations of photoperiodically induced fattening in migratory blackheaded bunting (Emberiza melanocephala)(Ayes)

The body fattening and weight gain preceding vernal migration in birds is timed by a set of environmental factors of which daylength is predominant. However, the mechanism(s) by which these events is determined is poorly understood. Previous investigations on a photoperiodic migratory species, the blackheaded bunting ( Emberiza melanocephala ), indicate the involvement of a light-sensitive circadian rhythm during initiation of fat deposition and body weight gain. This communication presents data from another set of experiments aimed to characterize further the mechanism(s) of fat deposition in the same species.
Groups of photosensitive, unstimulated and stimulated birds were subjected to transfer and superimposition experiments for 30 days. While the former set included shifting of long-day (LD) birds to DD, SD (short days), DD/LD and SD/LD, in the latter a 90-minute bright light was superimposed at two different times of the day during the dim-green lighted phase 15L:9D of varying intensity. Birds were weighed at the beginning and at the end of experiments. Those in transfer cycles were also weighed at 10-day intervals. The results suggest that the premigratory body fattening and weight gain in blackheaded buntings is light dependent and timed by environmental daylength in accordance with the photosensitive endogenous circadian rhythm (ECR). They also show that the photoperiodic responses in birds in general are mediated by circadian rhythm(s).     

Seasonal, tissue-specific regulation of Akt/protein kinase B and glycogen synthase in hibernators

Yellow-bellied marmots (Marmota flaviventris) exhibit a circannual cycle of hyperphagia and nutrient storage in the summer followed by hibernation in the winter. This annual cycle of body mass gain and loss is primarily due to large-scale accumulation of lipid in the summer, which is then mobilized and oxidized for energy during winter. The rapid and predictable change in body mass makes these animals ideal for studies investigating the molecular basis for body weight regulation. In the study described herein, we monitored seasonal changes in the protein levels and activity of a central regulator of anabolic metabolism, the serine-threonine kinase Akt-protein kinase B (Akt/PKB), during the months accompanying maximal weight gain and entry into hibernation (June-November). Interestingly, under fasting conditions, Akt/PKB demonstrated a tissue-specific seasonal activation. Specifically, although Akt/PKB levels did not change, the activity of Akt/PKB (isoforms 1/alpha and 2/beta) in white adipose tissue (WAT) increased significantly in July. Moreover, glycogen synthase, which lies downstream of Akt/PKB on a linear pathway linking the enzyme to the stimulation of glycogen synthesis, demonstrated a similar pattern of seasonal activation. By contrast, Akt/PKB activity in skeletal muscle peaked much later (i.e., September). These data suggest the existence of a novel, tissue-specific mechanism regulating Akt/PKB activation during periods of marked anabolism.     

Factors Affecting Date of Implantation,Parturition, and Den Entry Estimated from Activity and Body Temperature in Free-Ranging Brown Bears

Knowledge of factors influencing the timing of reproduction is important for animal conservation and management. Brown bears (Ursus arctos) are able to vary the birth date of their cubs in response to their fat stores, but little information is available about the timing of implantation and parturition in free-ranging brown bears. Body temperature and activity of pregnant brown bears is higher during the gestation period than during the rest of hibernation and drops at parturition. We compared mean daily body temperature and activity levels of pregnant and nonpregnant females during preimplantation, gestation, and lactation. Additionally we tested whether age, litter size, primiparity, environmental conditions, and the start of hibernation influence the timing of parturition. The mean date of implantation was 1 December (SD = 12), the mean date of parturition was 26 January (SD = 12), and the mean duration of the gestation period was 56 days (SD = 2). The body temperature of pregnant females was higher during the gestation and lactation periods than that of nonpregnant bears. The body temperature of pregnant females decreased during the gestation period. Activity recordings were also used to determine the date of parturition. The parturition dates calculated with activity and body temperature data did not differ significantly and were the same in 50% of the females. Older females started hibernation earlier. The start of hibernation was earlier during years with favorable environmental conditions. Dates of parturition were later during years with good environmental conditions which was unexpected. We suggest that free-ranging pregnant brown bears in areas with high levels of human activities at the beginning of the denning period, as in our study area, might prioritize investing energy in early denning than in early parturition during years with favorable environmental conditions, as a strategy to prevent disturbances caused by human.