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.     

Time allocation of daily behaviors in subtropical passerine finch,spotted munia (Lonchura punctulata)

In birds, daily behavioral patterns that occur in response to intrinsic and extrinsic stimuli help us to understand the influence of ecological factors on them. The time allotment for an activity is important to maintain energy budget and maximize the chances of survival. In this study, we monitored daily patterns of flying/hopping and feeding/drinking behaviors through a video camera in spotted munia (Lonchura punctulata) maintained in 12L:12D. The results showed that munia is diurnal and shows bimodal pattern of all behaviors except feeding which was trimodel. The flying and hopping had similar amplitude, but feeding frequency was higher than drinking. The time allocation was maximum for flying/hopping followed by feeding and then drinking. The results suggest that daily behaviors in munia occur in patterns and have a timing component.     

Endogenous gonadal,LH and molt rhythms in tropical stonechats: effect of pair bond on period,amplitude, and pattern of circannual cycles

To investigate the effects of reproduction and associated stimuli on the circannual cycles of African stonechats Saxicola torquata axillaris birds were held for 29 months in aviaries under a constant equatorial (12.25 h) photoperiod, either singly (10 females and 10 males) or in 10 male/female pairs. The birds of all 3 groups went through circannual cycles in gonadal size, plasma LH and molt, but groups differed with regard to actual reproductive performance. During the second cycle, only one of the singly-held females laid eggs and incubated. In constrast, in the paired females egg-laying and incubation occurred in all but one bird. About 50% of the clutches from paired females contained fertilized eggs confirming the expectation of behavioral differences between the paired and unpaired birds. However, despite differences in reproductive performance there were no differences in either circannual period or duration of reproductive phases. Moreover, there was no correlation between number of broods produced per season and circannual parameters of the paired females. Therefore, the temporal course and, particularly, the period during which reproduction is possible is rigidly determined by an endogenous program that is not influenced by reproductive performance. A rigid program of this kind may be advantageous in the tropics because it prevents prolongation of the breeding season in years with favourable conditions which in turn could jeopardize optimal timing of breeding in the following year and thus reduce lifetime reproductive success.     

Evidence of an endogenous circannual rhythm in growth-rates in dinoflagellates

Prorocentrum micans and Gonyaulax excavata clonal cultures grown under constant laboratory environmental conditions (continuous light and 20 +/- 1 degree C), over a two-year period, exhibit significative changes in growth rate. When rhythmometrically analyzed by cosinor, a pattern resembling a circannual rhythm became apparent. Significant rhythmometric differences appeared between species. Endogenous rhythms of microorganisms may have ecological implications.     

Control of annual gonadal cycles in Indian songbirds

Abstract

Reproduction is a part of life cycle with great environmental dependence. In contrast to temperate avian species, which mostly breed during summer, the Indian songbirds have more flexible breeding programs and exhibit a spectrum of reproductive strategies with the breeding season scattered all over the year. Control of breeding cycles in the Indian songbirds, therefore, are broadly viewed in light of two strategies (i) birds showing strong photoperiodic component in regulation of reproductive and post-reproductive events (ii) birds that do not exhibit typical photoperiodic regulation indicating the involvement of an inherent rhythm of reproduction. Both circadian and circannual rhythms have been demonstrated to regulate annual gonadal cycles of Indian songbirds. While photoperiod continues to be a predominant proximate factor for timing of breeding in majority of Indian songbirds investigated so far, some studies reveal the role of non photoperiodic cues such as the food availability, temperature, rainfall, etc. in timing/modulating the timing of breeding. The conversion or non-conversion of thyroxine to triiodothyronine may act as a long or short photoperiod signal and may up or downregulate the synthesis and release of GnRH-I in hypothalamus, FSH and LH in anterior pituitary and gonadal steroids in gonads causing gonadal growth or regression, respectively.     

Evidence for the role of light intensity in the seasonal testicular cycle of a wild bird,black headed munia

Abstract

The effects of various light intensity levels (0.11, 0.48, 0.96 and 1.86 mW/cm²) of constant white light on the testicular cycle of a wild bird, Black headed munia were investigated. While in higher intensity (0.96 and 1.86 mW/cm²) treated birds precocious gonadal development was observed, low intensity illumination prevented gonadal regression, indicating a better maintenance of testicular activity under low intensity lighting in Black headed munia. Since the total hours of light exposure (24 hr/day) were the same for all the four experimental groups, and higher intensities could not prevent gonadal regression, it would seem that light intensity is more important than the hours of illumination in the reproduction of this bird.     

Scoto/photo‐periodic responses of a sub‐tropical finch (Spotted munia) in relation to seasonal breeding cycle

Abstract

Effects of continuous light and dark periods and long and ultrashort photoperiods on the gonadal function of a subtropical finch, Spotted munia, hitherto considered “non‐photosensitive”, were studied. This bird seems to be unique in that while gametogenesis and hormone production are stimulated by the continuous or long scoto periods the endogenous rhythm of reproduction continues in constant 24hr or 15hr long daily photoperiod.     

Increased p27, an essential component of cell cycle control,in Alzheimer's disease

A number of recent findings have demonstrated re-expression of cell cycle-related proteins in vulnerable neurones in Alzheimer's disease. We hypothesize that this attempt by neurones to re-enter mitosis is a response to external growth stimuli that leads to an abortive re-entry into the cell cycle and, ultimately, neuronal degeneration. In this study, to further delineate the role of mitotic processes in the pathogenesis of Alzheimer's disease, we investigated p27, a cyclin-dependent kinase inhibitor that plays a negatively regulatory role in cell cycle progression that, once phosphorylated at Thr187, is degraded via an ubiquitin-proteasome pathway. Here we report that both p27 and phosphorylated p27 (Thr187) show increases in the cytoplasm of vulnerable neuronal populations in Alzheimer's disease vs. age-matched control subjects. Importantly, phosphorylated p27 (Thr187) shows considerable overlap with tau-positive neurofibrillary pathology, including neurofibrillary tangles, dystrophic neurites and neuropil threads. The findings presented here suggest that dysregulation of the cell cycle plays a crucial role in the pathogenesis of Alzheimer's disease that may provide a novel mechanistic basis for therapeutic intervention.     

No evidence for melatonin-linked immunoenhancement over the annual cycle of an avian species

The winter immunoenhancement hypothesis associates long nights and increased exposure to melatonin with enhanced immune function in winter when resource availability is low and the chances of becoming ill are high. Thus, increased exposure to melatonin in the winter could be adaptive for species facing difficult winter conditions. This idea has found some support in studies of resident mammals. In birds, the link between day length and melatonin over the annual cycle is weaker, and contributions of melatonin to seasonal timing are unclear. Furthermore, many species, especially migrants, do not experience the most difficult conditions of their annual cycle in winter. In this study, we tested whether the winter immunoenhancement hypothesis holds in an avian species, the red knot Calidris canutus. We found that melatonin duration and amplitude varied significantly over the annual cycle with the highest values occurring in winter. However, peaks did not correspond to the winter solstice or with annual variation in immune function. Our findings do not support the winter immunoenhancement hypothesis in knots and question whether the idea that immune function should be bolstered in winter can be generalized to systems where winter is not the most difficult time of the year.     

Evidence for an intracellular sulfur cycle in cucumber leaves

H₂S emission from cucumber (Cucumis sativus L.) leaf discs supplied with L-cysteine in the dark is inhibited 80–90% by aminooxyacetic acid (AOA), an inhibitor of pyridoxal-phosphate dependent enzymes. Exposure to L-cysteine in the light enhanced the emission of H₂S in response to this sulfur source. Turning off the light reduced the emission of H₂S to the rate observed in continuous dark; turning on the light enhanced the emission of H₂S to the rate observed in continuous light. Therefore, in the light H₂S emission in response to L-cysteine becomes a partially light-dependent process. Treatment with cyanazine, an inhibitor of photosynthetic electron transport, reduced H₂S emission in the light to the rate observed in continuous dark, but did not affect H₂S emission in the dark. In leaf discs pre-exposed to L-cysteine in the light, treatment with cyanazine+ AOA inhibited the emission of H₂S in response to L-cysteine completely. Therefore, only part of the H₂S emitted in response to this sulfur source is derived from a light-independent, but pyridoxal-phosphate-dependent process; the balance of the H₂S emitted is derived from a light-dependent process that can be inhibited by cyanazine. When cucumber leaf discs were supplied with a pulse of L-[^35S]cysteine, radioactively labeled H₂S was emitted in two waves, one during the first hour of exposure to L-cysteine, and a second after 3–4 h; unlabeled H₂S, however, was emitted continuously. The second wave of emission of labeled H₂S was not observed in pulse-chase experiments in which sulfate or cyanazine were added to the treatment solution after 3 h of exposure to L-cysteine, or when the lights was turned off. The labeling pattern of sulfur compounds inside cucumber cells supplied with a pulse of L-[³⁵S]cysteine showed that the labeled H₂S released from L-cysteine partially enters first the sulfite, then the sulfate pool of the cells. The radioactively labeled sulfate, however, is not incorporated into L-cysteine, but enters the H₂S pool of the cells again. These observations are consistent with the idea of an intracellular sulfur cycle in plant cells. The L-cysteine taken up by the leaf discs seems to be desulfhydrated in a light-independent, but pyridoxal-phosphate-dependent process. The H₂S synthesized this way may be partially released into the atmosphere; the other part of the H₂S produced in response to L-cysteine may be oxidized to sulfite, then to sulfate, which is subsequently reduced via the light-depent sulfate assimilation pathway. In the presence of excess L-cysteine, synthesis of additional cysteine may be inhibited, and the sulfide moiety may be split off carrier bound sulfide to enter the H₂S pool of the cells again. It is suggested that the function of this sulfur cycle may be regulation of the free cysteine pool.Abbreviation AOA aminooxyacetic acid     

Transmission of influenza reflects seasonality of wild birds across the annual cycle

Influenza A Viruses (IAV) in nature must overcome shifting transmission barriers caused by the mobility of their primary host, migratory wild birds, that change throughout the annual cycle. Using a phylogenetic network of viral sequences from North American wild birds (2008–2011) we demonstrate a shift from intraspecific to interspecific transmission that along with reassortment, allows IAV to achieve viral flow across successive seasons from summer to winter. Our study supports amplification of IAV during summer breeding seeded by overwintering virus persisting locally and virus introduced from a wide range of latitudes. As birds migrate from breeding sites to lower latitudes, they become involved in transmission networks with greater connectivity to other bird species, with interspecies transmission of reassortant viruses peaking during the winter. We propose that switching transmission dynamics may be a critical strategy for pathogens that infect mobile hosts inhabiting regions with strong seasonality.     

Short-day experience is not a prerequisite for the termination of photorefractoriness in the reproductive cycle of baya weaver,Ploceus philippinus

In most photoperiodic avian forms (irrespective of temperate or tropical distribution) including the baya weaver,Ploceus philippinus, seasonal reproduction comes to an end due to the development of a photoperiodically controlled photorefractory phase when birds cease to respond to the stimulatory effect of long days. In the present paper photoperiodic control of the termination of photorefractory phase has been examined by studying the effect of short-day exposure lasting 4–6 months on long-day response of birds. Results indicate that unlike in other photoperiodic birds short-day exposure of winter is not a prerequisite for the termination of photorefractory phase in the reproductive cycle of baya weaver. Artificial long days on the other hand hasten the termination of this phase. Refractory phase in baya weaver, therefore, unlike that in temperate forms, is a temporary state resulting most likely from a sequel of physiological events triggered by long days of spring/summer which temporarily mask the photostimulatory response. Spontaneous termination of photorefractoriness in birds of tropical habitats may have a selective value imparting to the reproductive cycle the necessary elasticity for adaptation to diverse ecological conditions.     

Photoperiodic requirements for timing onset and duration of the breeding season of the ewe: Synchronization of an endogenous rhythm of reproduction

Summary A study was conducted to test the hypothesis that different portions of the annual photoperiodic cycle play different roles in timing the breeding season of the ewe, Ovis aries, an animal in which an endogenous rhythm generates the seasonal reproductive transitions. Adult female sheep were pinealectomized to disrupt transduction of photoperiodic cues at 4 times of the year (summer and winter solstices, vernal and autumnal equinoxes), and the effects on seasonal reproductive neuroendocrine activity were evaluated. Time of pinealectomy greatly influenced the subsequent seasonal reproductive cycle such that the following inferences are possible. Lengthening days between the winter and summer solstices synchronize reproductive onset to the appropriate time of year. The relatively long days around the summer solstice act to suppress reproductive activity and forestall the start of the breeding season until late summer/early autumn. The shortening days between the summer solstice and autumnal equinox maintain a normal intensity and duration of reproductive neuroendocrine induction during the impending breeding season. However, the shortening days between the autumnal equinox and winter solstice (i.e., after breeding season onset) do not appear to play a critical role in maintaining the breeding season of that year, but may provide important cues for timing the breeding season of the following year.Abbreviations LH luteinizing hormone Presented in preliminary form at the 21st Annual Meeting of the Society for the Study of Reproduction, 1988, Biol Reprod 38 (Suppl. 1): 184 (Abstract 408). This work was performed in partial fulfillment of the requirements for the degree of Ph.D. at The University of Michigan (to N.L.W.), and was funded by NIH-HD-18337 and NIH-HD-18258, T-32-HD-07048, the Institut National de la Recherche Agronomique (France) and the Office of the Vice President for Research of The University of Michigan.