Daily levels and rhythm in circulating corticosterone and insulin are altered with photostimulated seasonal states in night-migratory blackheaded buntings

The circadian rhythms are involved in the photostimulation of seasonal responses in migratory blackheaded buntings. Here, we investigated whether changes in daily levels and rhythm in corticosterone (cort) and insulin secretions were associated with transitions in the photoperiodic seasonal states. Buntings were exposed to short days to maintain the winter (photosensitive) non-migratory state, and to long days for varying durations to induce the premigratory, migratory (shown by migratory restlessness at night, Zugunruhe) and summer non-migratory (photorefractory) states. We monitored activity patterns, and measured plasma cort and insulin levels at six and four times, respectively, over 24 h in each seasonal state. Buntings were fattened and weighed heavier, and exhibited intense nighttime activity in the migratory state. The daytime activity patterns also showed seasonal differences, with a bimodal pattern with morning and evening activity bouts only in the summer non-migratory state. Further, the average baseline hormone levels were significantly higher in premigratory and migratory than in the winter non-migratory state. Both cort and insulin levels showed a significant daily rhythm, but with seasonal differences. Whereas, cort rhythm acrophases (estimated time of peak secretion over 24 h) were at night in the winter non-migratory, premigratory and migratory states, the insulin rhythm acrophases were found early in the day and night in winter and summer non-migratory states, respectively. These results suggest that changes in daily levels and rhythm in cort and insulin mediate changes in the physiology and behavior with photostimulated transition in seasonal states in migratory blackheaded buntings.     

Life at a different pace: Annual itineraries are conserved in seasonal songbirds

The duration of life history state (LHS) reflects the adaptive strategy a species has evolved to cope with a changing environment. Inhabitants at different latitudes may thus have significant differences in the rates of metabolic and physiological processes underlying LHSs. Birds, in order to maximize their fitness in the environment in which they live, seasonally switch from one LHS to another during the year. The present study investigated whether an annual itinerary of a species would determine its rate of reaction to inductive long days. We compared the photoinduced cycles of changes in body mass and testes, as indices of migratory and reproductive LHSs, between two long day breeding species, the migratory redheaded bunting and non-migratory Indian weaverbird. Changes in body mass and testis size were measured in photosensitive buntings and weaverbirds (n = 7 each) on short days (LD 8:16) subjected first to 0.5 h weekly light increments until the light period was 13 h per day, and then maintained on LD 13:11 for another 32 weeks. A similar observation was recorded on a group of buntings (n = 14) and weaverbirds (n = 9) maintained on increasing natural day lengths (NDL; Lucknow, 26°55' N, 80°59' E) for 47 weeks. As predicted, the rates of induction of seasonal cycles under an identical inductive photoperiod were significantly faster in temperate buntings with five annual LHSs than in the subtropical weaverbirds with three annual LHSs. This suggests that annual itineraries of songbirds with which they may have evolved with at their breeding latitudes, determine their response to the external photoperiodic environment.     

Patterns of wheel running are related to Fos expression in neuropeptide-Y-containing neurons in the intergeniculate leaflet of Arvicanthis niloticus

A variety of nonphotic influences on circadian rhythms have been documented in mammals. In hamsters, one such influence, running in a novel wheel, is mediated in part by the pathway extending from neuropeptide-Y (NPY)-containing cells within the intergeniculate leaflet (IGL) of the thalamus to the hypothalamic suprachiasmatic nucleus (SCN). Arvicanthis niloticus is a species in which all individuals are diurnal with respect to general activity and body temperature when they are housed without a running wheel, but access to a running wheel induces a subset of individuals to become nocturnal. In the first study, the authors evaluated the possibility that nocturnal and diurnal patterns of wheel running in Arvicanthis are correlated with differences in IGL function. Adult male Arvicanthis housed in a 12:12 light-dark (LD) cycle were monitored in wheels, classified as nocturnal or diurnal, and then perfused either 4 h after lights-on or 4 h after lights-off. Sections through the intergeniculate leaflet were processed for immunohistochemical labeling of Fos and NPY. The percentage of NPY cells that expressed Fos was significantly influenced by an interaction between time of day and phenotype such that it rose from night to day in diurnal animals, and from day to night in nocturnal animals. In the second experiment, the authors established that running in a wheel actually induces Fos in the IGL of Arvicanthis. Specifically, the proportion of NPY cells expressing Fos was increased by access to wheels in nocturnal animals at night and in diurnal animals during the day. In the third experiment, the authors established that lesions of the IGL eliminate NPY fibers within the SCN, suggesting that these IGL cells project to the SCN in this species as has been established in other rodents. Together, these data demonstrate a clear difference in NPY cell function in nocturnal and diurnal Arvicanthis that appears to be caused, at least in part, by the differences in their wheel-running patterns, and that NPY cells within the IGL project to the SCN in Arvicanthis.     

Biochronometry of photoperiodically induced fat deposition in a migratory finch, the Blackheaded bunting (Emberiza melanocephala) (Aves)

This investigation attempts to identify the mechanism(s) involved in the fat deposition in a photoperiodic migratory species, the Blackheaded bunting ( Emberiza melanocephala ). Groups of photosensitive male buntings were exposed to resonance, interrupted night, and ultra-short-day light cycles for 35, 42 and 75 days, respectively. Birds were weighed at the beginning and at the end of the experiments. Those exposed to ultra-short-day light cycles were also weighed at critical intervals during the treatment period. Our results indicate that: (a) a light-sensitive rhythm with a period of about 24 hr is involved in the photoperiodic induction of premigratory fattening and weight gain in Blackheaded buntings: (b) buntings possess a bimodal pattern 'of sensitivity to photoperiods that induce fattening, and (c) this endogenous circadian rhythm can be entrained by an ultrashort photophase of 3 h if the latter is coupled with scotophases of specific duration.     

Circadian organization in male mice lacking the gene for endothelial nitric oxide synthase (eNOS-/-)

Circadian (approximately 24 h) rhythms in physiology and behavior are generated by the bilateral suprachiasmatic nucleus (SCN) of the anterior hypothalamus. For these endogenous rhythms to be synchronized with the external environment, light information must be transmitted to pacemaker cells within the SCN. This transmission of light information is accomplished via a direct retino-hypothalamic tract (RHT). Nitric oxide (NO), an endogenous gas that functions as a neurotransmitter, has been implicated as a messenger necessary for photic entrainment. Three isoforms of the enzyme that form NO, NO synthase, have been identified (a) in neurons (nNOS), (b) in the endothelial lining of blood vessels (eNOS), and (c) as an inducible form in macrophages (iNOS). The present study was undertaken to determine the specific role of eNOS in circadian organization and photic entrainment. Wild-type (WT) and eNOS-/- mice were initially entrained to a 14:10 light:dark (LD) cycle. After 3 weeks, the LD cycle was phase advanced. After an additional 3 weeks, animals were held in constant darkness (DD). eNOS-/- animals did not exhibit a deficit in the ability to entrain to the LD cycle, phase-shift locomotor activity, or free-run in constant conditions. Animals held in DD were killed after light exposure during either the subjective day or the subjective night to assess c-fos induction in the SCN. Light exposure during the subjective night increased c-fos protein expression in the SCN of both WT and eNOS-/- mice relative to animals killed after light exposure during the subjective day. Taken together, these findings suggest that endothelial isoform of NOS may not be necessary for photic entrainment in mice.     

Seasonal modulation of diurnal food consumption in Indian songbirds

Seasonal changes in daily food consumption have a direct bearing with energy requirement of bird that is in turn associated with life history stage of birds. We compared seasonal changes in daily food intake in adult male migratory redheaded bunting (Emberiza bruniceps) that over winters in Indian subcontinent with those in non-migratory blackheaded munia to reiterate the same. We also compared daily food eating pattern (DFEP) in wintering blackheaded and redheaded buntings, closely related Emberizidae finches to establish circadian nature of feeding behavior and how it varied at species level. The birds were held under short days (8L:16D; 8 h of light and 16 h of darkness) and two hourly food consumption was measured to profile their DFEP. Further, we extended the study to establish how the circadian pattern of food consumption varied depending on birds’ physiological state and effect of photoperiod in adult male redheaded buntings. Redheaded buntings DFEP and locomotor activity were compared in pre-migratory months of February (spring) and September (autumn). The results suggest that September (photorefractory) birds exhibit clear bimodality in their feeding behavior as compared to (photosensitive) birds in February. Another experiment compared bird’s DFEP held under short (8L:16D) and long (16L:8D) days for 5 weeks and suggested that under long days, prolonged hours of photophase render adaptive advantage to birds for positive energy budgeting. The present study clearly establishes the circadian nature of feeding behavior and that it modulates over seasons. The bimodal i.e. morning and evening peaks of food consumption suggest morning–evening food entrainable oscillators, however this needs to be investigated with mechanistic approach in future studies.     

Ovigerity,selective predation,and variable diel vertical migration in Euchaeta elongata (Copepoda: Calanoida)

Summary We present a statistical analysis of a previously published (Yen, 1983) but heretofore unanalyzed data set on the vertical distributions and diel vertical migration (DVM) of adult females of the marine planktonic copepod Euchaeta elongata in Dabob Bay, Washington, USA. Non-ovigerous females were strongly migratory on all four dates sampled, residing between 75–175 m during the day and at shallower depths during the night, commonly entering the upper 50 m of the water column. In contrast, ovigerous females were non-migratory or weakly migratory, largely remaining between 100–175 m both day and night, and entering the upper 50 m of the water column only rarely. Thus non-ovigerous females always migrated much more strongly, as measured by both amplitude of migration and the proportion of animals migrating, than did ovigerous females. These results led us to hypothesize that differential susceptibility to visually orienting predators was the cause of these differences in DVM behavior in female E. elongata, and we subsequently undertook an experimental study of the feeding selectivity of the copepod's natural predator, Pacific herring (Clupea harengus pallasi). Pacific herring exhibited a highly significant preference for ovigerous over nonovigerous adult female E. elongata. The demographic consequences of variable DVM in adult female E. elongata were investigated by way of life table analyses. Results indicated that under conditions of thermal stratification of the water column there is a distinct demographic disadvantage (reduced rate of realized population growth) incurred by non-migratory or weakly migratory ovigerous females due to delayed egg development at cooler subsurface temperatures. We conclude that ovigerous female E. elongata remain at depth both day and night to avoid visually orienting predators, and that such behavior must afford the copepod a demographic advantage of no less than a 26% reduction in adult mortality to offset the demographic cost of delayed egg development.     

Moult in captive partially migratory and sedentary Australian silvereyes ( Zosterops lateralis ) (Zosteropidae)

In this study, we describe and compare the duration and timing of post-breeding moult of primary and secondary wing feathers, tail feathers, wing coverts and body feathers in captive partially migratory and non-migratory Australian silvereyes (Zosterops lateralis). This study allowed us to follow individual birds through the course of their moult and record the progression of moult in two populations. Both groups of birds underwent a conventional (or basic) post-breeding moult. While all birds followed a similar pattern of feather replacement, differences were found in the timing and duration of moult between migratory and non-migratory birds. The migratory birds generally started their moult earlier in the year and completed it before the non-migratory birds. The migratory birds revealed an overall uniformity in the timing and duration of their moult, while the non-migratory birds showed a greater degree of variability between individuals.     

Photoperiodism and seasonality in neotropical population of Plutella xylostella L. (Lepidoptera: Yponomeutidae)

Neotropical populations of the diamondback moth Plutella xylostella L. have seasonal cycles of growth and decrease, and moth migration plays a fundamental role in generating such population dynamics. Since the oscillation of these populations is predictable, photoperiod might operate as a signal that triggers the migratory behaviour of the insect. Migration in insects is usually preceded by reproductive diapause, a photoperiodic response that can be characterised by morphological, physiological and behavioural alterations that permit to discriminate between migratory and non-migratory forms. In this study, I tested whether the pre-imaginal and reproductive development of P. xylostella from Minas Gerais (Brazil) is affected by artificial day-lengths that are equivalent to the periods of natural population growth or decrease. No evidence of photoperiodic response was found for the insect reared in laboratory on five different constant photoperiods, from 8h to 16h of light per day. There was no significant variation in survival and duration of egg, larva, and pupa stages or in pupal weight, adult size (forewing length), fecundity, and longevity. Although some species have geographically distinct photoperiodic responses, previous assumptions that cosmopolitan P. xylostella responds to photoperiod in temperate regions was questioned. Migratory and population seasonality among neotropical populations of P. xylostella certainly occurs independently of the photoperiodic announcement of seasonal changes in habitat quality.     

Cell activation in the hypothalamus after exposure to an antigen (based on c-fos gene expression)

Increase of the c-fos mRNA positive cells number was insignificant in 30 min. following activation of the rat hypothalamic structures with the tetanus toxoid (TT). Elevation of the c-fos mRNA positive cells number occurred in the hypothalamic' posterior (PHA), lateral (LHA), anterior (AHA), areas dorsomedial (DMH), and ventromedial (VMH) nuclei within 2 hours of the TT administration. In 6 hours the c-fos mRNA positive cells number decreased in PHA, LHA, DMH. The c-fos mRNA expression was stable in arquate and supraoptic hypothalamic nuclei following either the TT or saline administration.     

A putative suprachiasmatic nucleus of birds responds to visual motion

In mammals, the suprachiasmatic nucleus (SCN) is a pacemaker regulating daily rhythms. In birds, two retinorecipient nuclei have been called the avian SCN, one in the lateral hypothalamus and the other more medial and rostral. We asked whether the protooncogene c-fos is expressed in either nucleus after light exposure during subjective night, but not during subjective day, as is the case in the SCN of mammals.Chicks raised with one eye covered by a diffuser were exposed to vertically moving surroundings, after the difuser had been switched to the other eye.Surprisingly, we saw strong Fos label only in the lateral nucleus contralateral to the eye newly exposed to visual motion, but not in the ipsilateral nucleus nor in either medial SCN. No label was seen in animals kept in darkness or if the diffuser was not switched. Fos labeling did not differ between subjective day and night. The sensitivity to novel motion is also seen in motion-processing nuclei of the accessory optic system and pretectum; this suggests either that the lateral SCN is not the SCN, but part of the motion pathway, or that the avian SCN may be motion-sensitive during both day and night.     

Neuropeptide Y–Induced Phase Shifts of PER2::LUC Rhythms Are Mediated by Long-Term Suppression of Neuronal Excitability in a Phase-Specific Manner

Endogenous circadian rhythms are entrained to the 24-h light/dark cycle by both light and nonphotic stimuli. During the day, nonphotic stimuli, such as novel wheel-induced exercise, produce large phase advances. Neuropeptide Y (NPY) release from the thalamus onto suprachiasmatic nucleus (SCN) neurons at least partially mediates this nonphotic signal. The authors examined the hypothesis that NPY-induced phase advances are accompanied by suppression of PER2 and are mediated by long-term depression of neuronal excitability in a phase-specific manner. First, it was found that NPY-induced phase advances in PER2::LUC SCN cultures are largest when NPY (2.35 µM) is given in the early part of the day (circadian time [CT] 0–6). In addition, PER2::LUC levels in NPY-treated (compared to vehicle-treated) samples were suppressed beginning 6–7?h after treatment. Similar NPY application to organotypic Per1::GFP SCN cultures resulted in long-term suppression of spike rate of green fluorescent protein–positive (GFP+) cells when slices were treated with NPY during the early or middle of the day (zeitgeber time [ZT] 2 or 6), but not during the late day (ZT 10). Furthermore, 1-h bath application of NPY to acute SCN brain slices decreased general neuronal activity measured through extracellular recordings. Finally, NPY-induced phase advances of PER2::LUC rhythms were blocked by latent depolarization with 34.5?mM K⁺ 3?h after NPY application. These results suggest that NPY-induced phase advances may be mediated by long-term depression of neuronal excitability. This model is consistent with findings in other brain regions that NPY-induced persistent hyperpolarization underlies mechanisms of energy homeostasis, anxiety-related behavior, and thalamocortical synchronous firing. (Author correspondence: klgamble@uab.edu)     

Circadian locomotor analysis of male mice lacking the gene for neuronal nitric oxide synthase (nNOS-/-)

Nitric oxide (NO) is an endogenous gas that functions as a neurotransmitter. Because NO is very labile with a half-life of less than 5 sec, most functional studies of NO have manipulated its synthetic enzyme, NO synthase (NOS). Three isoforms of NOS have been identified: (1) in the endothelial lining of blood vessels (eNOS), (2) an inducible form found in macrophages (iNOS), and (3) in neurons (nNOS). Most pharmacological studies to date have blocked all three isoforms of NOS. Previous studies using such agents have revealed that NO might be necessary for photic entrainment of circadian rhythms; general NOS inhibitors attenuate phase shifts of free-running behavior, light-induced c-fos expression in the suprachiasmatic nucleus (SCN), and phase shifts of neural firing activity in SCN maintained in vitro. To assess the specific role of nNOS in mediating entrainment of circadian rhythms, mice with targeted deletion of the gene encoding the neuronal isoform of NOS (nNOS-/-) were used. Wild-type (WT) and nNOS-/- mice initially were entrained to a 14:10 light:dark (LD) cycle. After 3 weeks, the LD cycle was either phase advanced or phase delayed. After an additional 3 weeks, animals were held in either constant dim light or constant dark. WT and nNOS-/- animals did not differ in their ability to entrain to the LD cycle, phase shift locomotor activity, or free run in constant conditions. Animals held in constant dark were killed after light exposure during either the subjective day or subjective night to assess c-fos induction in the SCN. Light exposure during the subjective night increased c-fos expression in the SCN of both WT and nNOS-/- mice relative to animals killed after light exposure during the subjective day. Taken together, these findings suggest that NO from neurons might not be necessary for photic entrainment.     

Daily light regulates seasonal responses in the migratory male redheaded bunting (Emberiza bruniceps)

This study analyzed the role of day length in regulation of seasonal body fattening and testicular growth in a latitudinal Palaearctic-Indian migrant, the redheaded bunting (Emberiza bruniceps). When exposed to increasing photoperiods (hours of light: hours of darkness; 11.5L:12.5D, 12L:12D, 12.5L:11.5D, 13L:11D, 14L:10D, and 18L:6D) for 9-12 weeks, buntings responded in a photoperiod-dependent manner and underwent growth and regression cycle under photoperiods of > or =12 hr per day. Also, the response to a long photoperiod of birds that were held under natural photoperiods at 27 degrees N for 2 years was similar to those who arrived the same year from their breeding grounds ( approximately 40 degrees N), suggesting that the experience of higher amplitude day-night (light-dark, LD) cycles during migratory and breeding seasons were not critical for the subsequent response (initiation-termination-reinitiation) cycle. Another experiment examined entrainment of the circadian photoperiodic rhythm in buntings by subjecting them to T=24+/-2 hr LD-cycles with 8 hr photophase and to T=22 and 24 hr with 11 hr photophase. The results showed a reduction in critical day length under T=22 hr LD-cycle. In the last experiment, we constructed an action spectrum for photoperiodic induction by exposing birds for 4.5 weeks to 13L:11D of white (control), blue (450 nm), or red (640 nm) light at irradiances ranging from 0.028 to 1.4 W m(-2). The threshold light irradiance for photoinduction was about 10-fold higher for blue light, than for red and white lights. These results conclude that the daily light of the environment regulates the endogenous program that times seasonal responses in body fattening and testicular cycles of the redheaded bunting.     

Altered light conditions during spring: effects on timing of migration and reproduction in migratory redheaded bunting (Emberiza bruniceps)

Photoperiod is the most consistent environmental cue, and therefore, any change in anticipated light environment may affect subsequent response under long days. To test this hypothesis, photosensitive migratory redheaded buntings (Emberiza bruniceps) were exposed to altered photoperiods for 4 weeks [short days (SP, 8L:16D, group 1; control), short days alternated with constant dim light (SP/LL_dim; group 2), constant dim light (LL_dim; group 3) and constant bright light (LL_bright; group 4)] before being transferred to long days (LP; 16L:8D) for 15 weeks. Group differences in long-day-induced responses were observed. The onset of migratory restlessness (Zugunruhe) was earliest in LL_bright but persisted for maximum period in LL_dim group. The LL_dim group attained peak testis size significantly delayed and had more food consumption under long days. The results suggest that the altered photoperiodic exposure during photosensitive stage affects the seasonal phenotypes such as migration and reproduction in migratory buntings.     

Circadian Integration of Glutamatergic Signals by Little SAAS in Novel Suprachiasmatic Circuits

Background

Neuropeptides are critical integrative elements within the central circadian clock in the suprachiasmatic nucleus (SCN), where they mediate both cell-to-cell synchronization and phase adjustments that cause light entrainment. Forward peptidomics identified little SAAS, derived from the proSAAS prohormone, among novel SCN peptides, but its role in the SCN is poorly understood.

Methodology/Principal Findings

Little SAAS localization and co-expression with established SCN neuropeptides were evaluated by immunohistochemistry using highly specific antisera and stereological analysis. Functional context was assessed relative to c-FOS induction in light-stimulated animals and on neuronal circadian rhythms in glutamate-stimulated brain slices. We found that little SAAS-expressing neurons comprise the third most abundant neuropeptidergic class (16.4%) with unusual functional circuit contexts. Little SAAS is localized within the densely retinorecipient central SCN of both rat and mouse, but not the retinohypothalamic tract (RHT). Some little SAAS colocalizes with vasoactive intestinal polypeptide (VIP) or gastrin-releasing peptide (GRP), known mediators of light signals, but not arginine vasopressin (AVP). Nearly 50% of little SAAS neurons express c-FOS in response to light exposure in early night. Blockade of signals that relay light information, via NMDA receptors or VIP- and GRP-cognate receptors, has no effect on phase delays of circadian rhythms induced by little SAAS.

Conclusions/Significance

Little SAAS relays signals downstream of light/glutamatergic signaling from eye to SCN, and independent of VIP and GRP action. These findings suggest that little SAAS forms a third SCN neuropeptidergic system, processing light information and activating phase-shifts within novel circuits of the central circadian clock.     

Distinct migratory and non-migratory ecotypes of an endemic New Zealand eleotrid (<Emphasis Type="Italic">Gobiomorphus cotidianus</Emphasis>) – implications for incipient speciation in island freshwater fish species

Background  

Many postglacial lakes contain fish species with distinct ecomorphs. Similar evolutionary scenarios might be acting on evolutionarily young fish communities in lakes of remote islands. One process that drives diversification in island freshwater fish species is the colonization of depauperate freshwater environments by diadromous (migratory) taxa, which secondarily lose their migratory behaviour. The loss of migration limits dispersal and gene flow between distant populations, and, therefore, is expected to facilitate local morphological and genetic differentiation. To date, most studies have focused on interspecific relationships among migratory species and their non-migratory sister taxa. We hypothesize that the loss of migration facilitates intraspecific morphological, behavioural, and genetic differentiation between migratory and non-migratory populations of facultatively diadromous taxa, and, hence, incipient speciation of island freshwater fish species.     

Migratory behavior of related moose

In a Swedish moose population containing both migratory and non-migratory individuals, 15 cows, 19 first generation and 2 second generation offspring were radiocollared and monitored during 1980–87 to determine their migratory behavior. The migratory behavior of offspring was evaluated when they were > 1 year old and independent of their dams. All 11 migratory cows produced migratory offspring (10♀, 3♂). Two migratory offspring produced female calves (grandchildren to the originally sampled cows) that were also migratory. Four of the originally sampled cows were non-migratory and they produced six non-migratory offspring (3♀, 3♂). Distances migrated by independent offspring were related to those of their dam. No moose changed its migrant or non-migrant nature during the study. Results indicate that the proportion of migratory moose in the population is determined by the survival and reproductive success of migratory versus non-migratory cows. Migratory and non-migratory moose may be regarded as two distinct phenotypes in this population.     

Differential responses of the photoperiodic clock in two passerine birds possessing a strongly self-sustained circadian system

To investigate whether the photoperiodic clocks of species possessing strongly self-sustaining circadian clocks share identical features, we compared the full response cycle (initiation and termination of the response) in body mass and testes of the non-migratory house sparrow (Passer domesticus) with that of the migratory redheaded bunting (Emberiza bruniceps) under Nanda-Hamner experiments. Birds were exposed to a 36 h day (L:D=6:30 h), controls exposed to a 24 h day (L:D=6:18 h), for a period of 31 weeks. By week 18 of L:D=6:18 h, there was a small increase in body mass among sparrows, but not among buntings, and the testes of bunting did not grow, while those of sparrow grew slightly. The response to L:D=6:30 h is of particular interest. There was a rapid gain and subsequent loss in the body mass of bunting, but not of sparrows. Further, both species underwent a testicular cycle as if they were exposed to long days, but the response of sparrows was slower and hence delayed the attainment of peak testicular size. Such a differential response to exotic light cycles between these two photosensitive species, despite their similar circadian oscillatory properties (strong self-sustainment), could suggest a species-specific adaptation of the endogenous clock involved in photoperiodic regulation of avian seasonality.