Peripheral melatonin modulates seasonal immunity and reproduction of Indian tropical male bird Perdicula asiatica

Seasonal changes in pineal function are well coordinated with seasonal reproductive activity of tropical birds. Further, immunomodulatory property of melatonin is well documented in seasonally breeding animals. Present study elucidates the interaction of peripheral melatonin with seasonal pattern of immunity and reproduction in Indian tropical male bird Perdicula asiatica. Significant seasonal changes were noted in pineal, testicular and immune function(s) of this avian species. Maximum pineal activity along with high immune status was noted during winter month while maximum testicular activity with low immune status was noted in summer. During summer month's long photoperiod suppressed pineal activity and high circulating testosterone suppressed immune parameters, while in winter short photoperiod elevated pineal activity and high circulating melatonin maintained high immune status and suppressed gonadal activity. Therefore, seasonal levels of melatonin act like a major temporal synchronizer to maintain not only the seasonal reproduction but also immune adaptability of this avian species.     

Melatonin mediates seasonal adjustments in immune function.

In addition to seasonal changes in reproductive function, seasonal changes in immune function are mediated by the pineal hormone, melatonin. Melatonin affects immune function both indirectly, acting through other hormones, and directly by acting on components of the immune system. Melatonin also affects tumorigenesis and tumor development. We hypothesize that many of the indirect effects of melatonin on immune function are mediated through glucocorticoids, and appear to be part of an integrated series of adaptations to manage energy. Direct effects of melatonin on immune function appear to be mediated by melatonin receptors on lymphatic tissue or on immune cells in circulation. Winter is energetically demanding and stressful; thermoregulatory demands typically increase when food availability decreases. Individuals would enjoy a survival advantage if seasonally recurring stressors could be anticipated and countered by bolstering immune function. To summarize, melatonin may be part of an integrative system to coordinate reproductive, immunologic and other physiological processes to cope successfully with energetic stressors during winter.     

Housing condition alters immunological and reproductive responses to day length in Siberian hamsters (Phodopus sungorus)

During winter, increased thermoregulatory demands coincide with limited food availability necessitating physiological tradeoffs among expensive physiological processes resulting in seasonal breeding among small mammals. In the laboratory, short winter-like day lengths induce regression of the reproductive tract, but also enhance many aspects of immune function. It remains unspecified the extent to which bolstered immune responses in short days represent enhanced immune function per se compared to long days or represents energetic disinhibition mediated by the regression of the reproductive tract. Cohabitation of male Siberian hamsters with intact female conspecifics can block short-day reproductive regression. We sought to determine whether female cohabitation could also block the enhanced immune function associated with short days. Adult male Siberian hamsters were housed in long or short day lengths in one of three housing conditions: (1) single-housed, (2) housed with a same sex littermate, or (3) housed with an ovariectomized female. Delayed-type hypersensitivity (DTH) responses were assessed after 8 weeks of photoperiod treatment. Housing with an ovariectomized female was not sufficient to block short-day reproductive regression, but prevented short-day enhancement of DTH responses. Housing with a male littermate did not alter reproductive or immune responses in either photoperiod. These data suggest that short day enhancement of immune function is independent of photoperiod-mediated changes in the reproductive system.     

Role of photoperiod and melatonin in seasonal acclimatization of the djungarian hamster,Phodopus sungorus

The Djungarian hamster,Phodopus sungorus, shows a clear annual cycle in some thermogenic parameters such as nonshivering thermogenesis (NST) and cold resistance. These seasonal changes were found to be basically controlled by natural changes in photoperiod. Further support for this view was obtained by exposing the hamsters to artificial long and short photoperiods.Implantation of melatonin during fall and winter results in an increased thermogenic capacity in both short and long day hamsters comparable to that shown by values of control hamsters exposed to short photoperiods during winter. This thermotropic action of melatonin and of short photoperiod could be found only in fall and winter whereas during spring and summer, melatonin, like photoperiod, had no influence on thermogenic capacities. These results show that the actions of melatonin and photoperiod vary with the season and that they depend upon the photoperiodic history of the hamsters. Our results further indicate that the pineal gland with its hormone melatonin is involved in mediation of photoperiodic control of seasonal acclimatization.     

Melatonin enhancement of splenocyte proliferation is attenuated by luzindole, a melatonin receptor antagonist

In addition to marked seasonal changes in reproductive, metabolic, and other physiological functions, many vertebrate species undergo seasonal changes in immune function. Despite growing evidence that photoperiod mediates seasonal changes in immune function, little is known regarding the neuroendocrine mechanisms underlying these changes. Increased immunity in short days is hypothesized to be due to the increase in the duration of nightly melatonin secretion, and recent studies indicate that melatonin acts directly on immune cells to enhance immune parameters. The present study examined the contribution of melatonin receptors in mediating the enhancement of splenocyte proliferation in response to the T cell mitogen Concanavalin A in mice. The administration of luzindole, a high-affinity melatonin receptor antagonist, either in vitro or in vivo significantly attenuated the ability of in vitro melatonin to enhance splenic lymphocyte proliferation during the day or night. In the absence of melatonin or luzindole, splenocyte proliferation was intrinsically higher during the night than during the day. In the absence of melatonin administration, luzindole reduced the ability of spleen cells to proliferate during the night, when endogenous melatonin concentrations are naturally high. This effect was not observed during the day, when melatonin concentrations are low. Taken together, these results suggest that melatonin enhancement of splenocyte proliferation is mediated directly by melatonin receptors on splenocytes and that there is diurnal variation in splenocyte proliferation in mice that is also mediated by splenic melatonin receptors.     

Photoperiodic regulation of behavioral responses to bacterial and viral mimetics: a test of the winter immunoenhancement hypothesis

Siberian hamsters (Phodopus sungorus) exhibit changes in immune function following adaptation to short photoperiods, including a marked attenuation of energetically expensive thermoregulatory and behavioral responses to gram-negative bacterial infections. Whether this seasonal attenuation of the immune response is idiosyncratic to gram-negative infections or is representative of innate immune responses in general is not known. If seasonal attenuation of responsiveness to infection is indeed driven primarily by anticipation of energetic constraints, then one would predict that responsiveness to all pathogens would be diminished during short days. If, on the other hand, seasonal changes in responsiveness to infection reflect anticipation of specific pathogens that are common at different phases of the annual cycle, then one would expect short photoperiods to attenuate responsiveness to some pathogens and long photoperiods to attenuate responsiveness to others. To resolve this issue, we exposed male Siberian hamsters to either long or short photoperiods for 11 weeks, then examined their behavioral sickness responses to compounds that represent the minimally immunogenic components of gram-negative bacterial (lipopolysaccharide), gram-positive bacterial (muramyl dipeptide), and viral (polyinosinepolycytidylic acid) organisms. Hamsters exhibited anorexic, anhedonic, ponderal, and/or thermoregulatory sickness behaviors to all 3 pathogen mimetics, but in all cases in which sickness responses were evident, they were attenuated in short days. Energetically costly behavioral responses to several distinct classes of infectious organisms are attenuated in anticipation of winter. The data are not consistent with a pathogen-specific seasonal modulation of innate immune responses.     

Global climate change and invariable photoperiods: A mismatch that jeopardizes animal fitness

The Earth's surface temperature is rising, and precipitation patterns throughout the Earth are changing; the source of these shifts is likely anthropogenic in nature. Alterations in temperature and precipitation have obvious direct and indirect effects on both plants and animals. Notably, changes in temperature and precipitation alone can have both advantageous and detrimental consequences depending on the species. Typically, production of offspring is timed to coincide with optimal food availability; thus, individuals of many species display annual rhythms of reproductive function. Because it requires substantial time to establish or re‐establish reproductive function, individuals cannot depend on the arrival of seasonal food availability to begin breeding; thus, mechanisms have evolved in many plants and animals to monitor and respond to day length in order to anticipate seasonal changes in the environment. Over evolutionary time, there has been precise fine‐tuning of critical photoperiod and onset/offset of seasonal adaptations. Climate change has provoked changes in the availability of insects and plants which shifts the timing of optimal reproduction. However, adaptations to the stable photoperiod may be insufficiently plastic to allow a shift in the seasonal timing of bird and mammal breeding. Coupled with the effects of light pollution which prevents these species from determining day length, climate change presents extreme evolutionary pressure that can result in severe deleterious consequences for individual species reproduction and survival. This review describes the effects of climate change on plants and animals, defines photoperiod and the physiological events it regulates, and addresses the consequences of global climate change and a stable photoperiod.     

Photoperiod differentially regulates circadian oscillators in central and peripheral tissues of the Syrian hamster

In many seasonally breeding rodents, reproduction and metabolism are activated by long summer days (LD) and inhibited by short winter days (SD). After several months of SD, animals become refractory to this inhibitory photoperiod and spontaneously revert to LD-like physiology. The suprachiasmatic nuclei (SCN) house the primary circadian oscillator in mammals. Seasonal changes in photic input to this structure control many annual physiological rhythms via SCN-regulated pineal melatonin secretion, which provides an internal endocrine signal representing photoperiod. We compared LD- and SD-housed animals and show that the waveform of SCN expression for three circadian clock genes (Per1, Per2, and Cry2) is modified by photoperiod. In SD-refractory (SD-R) animals, SCN and melatonin rhythms remain locked to SD, reflecting ambient photoperiod, despite LD-like physiology. In peripheral oscillators, Per1 and Dbp rhythms are also modified by photoperiod but, in contrast to the SCN, revert to LD-like, high-amplitude rhythms in SD-R animals. Our data suggest that circadian oscillators in peripheral organs participate in photoperiodic time measurement in seasonal mammals; however, circadian oscillators operate differently in the SCN. The clear dissociation between SCN and peripheral oscillators in refractory animals implicates intermediate factor(s), not directly driven by the SCN or melatonin, in entrainment of peripheral clocks.     

Photoperiodic control of seasonality in birds

This review examines how birds use the annual cycle in photoperiod to ensure that seasonal events--breeding, molt, and song production--happen at the appropriate time of year. Differences in breeding strategies between birds and mammals reflect basic differences in biology. Avian breeding seasons tend to be of shorter duration and more asymmetric with respect to changes in photoperiod. Breeding seasons can occur at the same time each year (predictable) or at different times (opportunistic), depending on the food resource. In all cases, there is evidence for involvement of photoperiodic control, nonphotoperiodic control, and endogenous circannual rhythmicity. In predictable breeders (most nontropical species), photoperiod is the predominant proximate factor. Increasing photoperiods of spring stimulate secretion of gonadotropin-releasing hormone (GnRH) and consequent gonadal maturation. However, breeding ends before the return of short photoperiods. This is the consequence of a second effect of long photoperiods--the induction of photorefractoriness. This dual role of long photoperiods is required to impart the asymmetry in breeding seasons. Typically, gonadal regression through photorefractoriness is associated with a massive decrease in hypothalamic GnRH, essentially a reversal to a pre-pubertal condition. Although breeding seasons are primarily determined by photoperiodic control of GnRH neurons, prolactin may be important in determining the exact timing of gonadal regression. In tropical and opportunistic breeders, endogenous circannual rhythmicity may be more important. In such species, the reproductive system remains in a state of "readiness to breed" for a large part of the year, with nonphotic cues acting as proximate cues to time breeding. Circannual rhythmicity may result from a temporal sequence of different physiological states rather than a molecular or cellular mechanism as in circadian rhythmicity. Avian homologues of mammalian clock genes Per2, Per3, Clock, bmal1, and MOP4 have been cloned. At the molecular level, avian circadian clocks appear to function in a similar manner to those of mammals. Photoperiodic time measurement involves interaction between a circadian rhythm of photoinducibility and, unlike mammals, deep brain photoreceptors. The exact location of these remains unclear. Although the eyes and pineal generate a daily cycle in melatonin, this photoperiodic signal is not used to time seasonal breeding. Instead, photoperiodic responses appear to involve direct interaction between photoreceptors and GnRH neurons. Thyroid hormones are required in some way for this system to function. In addition to gonadal function, song production is also affected by photoperiod. Several of the nuclei involved in the song system show seasonal changes in volume, greater in spring than in the fall. The increase in volume is, in part, due to an increase in cell number as a result of neurogenesis. There is no seasonal change in the birth of neurons but rather in their survival. Testosterone and melatonin appear to work antagonistically in regulating volume.     

Daily torpor in relation to photoperiod in a subtropical blossom-bat, Syconycteris australis (Megachiroptera)

Daily torpor in many temperate-zone mammals is affected by photoperiod. As little is known about the effects of photoperiod on torpor in subtropical species, we investigated whether, and if so how, torpor use, duration, and depth are affected by acclimation to three photoperiods (short, intermediate, long) in the blossom-bat Syconycteris australis. In contrast to many other studies, torpor occurrence, duration, and depth did not significantly respond to photoperiod acclimation in S. australis. Interestingly, the trend of a decline in torpor use under long photoperiod was the opposite of that observed previously in S. australis, which had been captured from the wild in summer and winter. Our study suggests that some species living in low latitude areas with unpredictable weather like S. australis may not use photoperiod for seasonal adjustments in physiology because it is not a reliable cue for food availability.     

Metabolic stress suppresses humoral immune function in long-day,but not short-day,Siberian hamsters (<Emphasis Type="Italic">Phodopus sungorus</Emphasis>)

Individuals of many species experience marked seasonal variation in environmental conditions and must adapt to potentially large fluctuations in energy availability and expenditure. Seasonal changes in immunity have likely evolved as an adaptive mechanism to cope with seasonal stressors. In addition, these changes may be constrained by seasonal fluctuations in energy availability. The goal of this study was to assess the role of energetic trade-offs associated with seasonal variation in immunity. In addition to body fat stores, metabolic fuels (e.g., glucose) may affect immune function in seasonally breeding rodents. In this study we experimentally reduced energy availability via injections of the metabolic inhibitor 2-deoxy-d-glucose (2-DG) in long- and short-day housed Siberian hamsters (Phodopus sungorus) and then examined antigen-specific antibody production. Metabolic stress decreased antibody response compared with control animals in long days. In contrast, no difference was observed between treatment groups in short days. These data suggest that reductions in energy availability suppress immunity and short days buffer organisms against glucoprivation-induced immunosuppression.     

Control of the annual cycle in birds: endocrine constraints and plasticity in response to ecological variability

This paper reviews information from ecological and physiological studies to assess how extrinsic factors can modulate intrinsic physiological processes. The annual cycle of birds is made up of a sequence of life-history stages: breeding, moult and migration. Each stage has evolved to occur at the optimum time and to last for the whole duration of time available. Some species have predictable breeding seasons, others are more flexible and some breed opportunistically in response to unpredictable food availability. Photoperiod is the principal environmental cue used to time each stage, allowing birds to adapt their physiology in advance of predictable environmental changes. Physiological (neuroendocrine and endocrine) plasticity allows non-photoperiodic cues to modulate timing to enable individuals to cope with, and benefit from, short-term environmental variability. Although the timing and duration of the period of full gonadal maturation is principally controlled by photoperiod, non-photoperiodic cues, such as temperature, rainfall or food availability, could potentially modulate the exact time of breeding either by fine-tuning the time of egg-laying within the period of full gonadal maturity or, more fundamentally, by modulating gonadal maturation and/or regression. The timing of gonadal regression affects the time of the start of moult, which in turn may affect the duration of the moult. There are many areas of uncertainty. Future integrated studies are required to assess the scope for flexibility in life-history strategies as this will have a critical bearing on whether birds can adapt sufficiently rapidly to anthropogenic environmental changes, in particular climate change.     

Seasonal changes in body mass, energy intake and thermogenesis in Maximowiczi’s voles (Microtus maximowiczii) from the Inner Mongolian grassland

Small mammals inhabiting temperate and arctic regions exhibit annual adaptive adjustments in physiology, anatomy, and behavior. No data on the physiology of Maximowicz’s voles (Microtus maximowiczii) are available at present. Here we examined the seasonal changes in body mass, food intake, thermogenic capacity, serum leptin and thyroid hormone levels in wild-captured individuals from Inner Mongolian grassland, China. We further examined the effects of photoperiod on these parameters. Energy intake, resting metabolic rate, nonshivering thermogenesis (NST), and serum tri-iodothyronine (T3) levels increased while serum leptin and body mass decreased in the cold seasons. Serum T3 levels were positively correlated with NST and uncoupling protein 1 (UCP1) contents in brown adipose tissue, and leptin levels were negatively correlated with energy intake and resting metabolic rate. Furthermore, laboratory data showed these changes could be induced by short photoperiod alone. Taken together, our results indicate that Maximowicz’s voles can increase thermogenic capacity and energy intake to cope with cold stress. Serum leptin seems to be involved in the regulation of energy intake and changes in T3 level may be important for the variations in NST and/or UCP1. Short photoperiod can serve as a seasonal cue for the winter acclimatization of energy balance in free-living Maximowicz’s voles.     

Leptin, but not immune function, is linked to reproductive responsiveness to photoperiod

Energetic demands are high while energy availability is minimum during winter. To cope with this energetic bottleneck, animals exhibit numerous energy-conserving adaptations during winter, including changes in immune and reproductive functions. A majority of individual rodents within a population inhibits reproductive function (responders) as winter approaches. A substantial proportion of small rodents within a species, however, fails to inhibit reproduction (nonresponders) during winter in the field or in the laboratory when maintained in winter-simulated day lengths. In contrast, immune function is bolstered by short day lengths in some species. The specific mechanisms that link reproductive and immune functions remain unspecified. Leptin is a hormone produced by adipose tissue, and several studies suggest that leptin modulates reproductive and immune functions. The present study sought to determine if photoperiodic alterations in reproductive function and leptin concentrations are linked to photoperiod-modulated changes in immune function. Siberian hamsters (Phodopus sungorus) were housed in either long (LD 16:8) or short (LD 8:16) day lengths for 9 wk. After 9 wk, blood samples were collected during the middle of the light and dark phase to assess leptin concentrations. One week later, animals were injected with keyhole limpet hemocyanin to evaluate humoral immunity. Body mass, body fat content, and serum leptin concentrations were correlated with reproductive responsiveness to photoperiod; short-day animals with regressed gonads exhibited a reduction in these measures, whereas short-day nonresponders resembled long-day animals. In contrast, immune function was influenced by photoperiod but not reproductive status. Taken together, these data suggest that humoral immune function in Siberian hamsters is independent of photoperiod-mediated changes in leptin concentrations.     

Food cues and gonadal development in neotropical spotted antbirds (Hylophylax naevioides)

Most temperate-zone birds live in environments with a regular seasonality, and primarily use the long-term changes in photoperiod as a cue to initiate gonadal development in anticipation of the breeding season. Short-term cues such as food and temperature are later used to fine-tune the rate of gonadal development to local conditions. Many tropical habitats are seasonal, but the timing of the seasons (e.g., rainy season) can vary considerably between years. We hypothesize that to time breeding in environments with seasonal variability, tropical birds respond to both long-term and short-term environmental cues to initiate gonadal growth. We tested the effectiveness of photoperiod and food cues for the initiation of gonad growth in captive male spotted antbirds (Hylophylax n. naevioides) from Panama. A ‘control’ group was maintained on the short natural photoperiod of 12 h light and 12 h dark (LD 12:12) and adequate food. A ‘food-stimulated’ group was also held on LD 12:12 but received an increase in food quantity and quality. A ‘photo+food-stimulated’ group experienced an increase in daylength by 1 h (LD 13:11, the maximal photoperiod in Panama) and an increase in food quantity and quality. Within 3 weeks testis sizes of ‘food-stimulated’ birds increased significantly, suggesting that food cues alone can initiate gonad development. As expected from the previous experiment, testis sizes of ‘photo+food-stimulated’ birds, but not ‘control’ birds, also increased. We suggest that the capability to respond to both food and photoperiodic cues allows animal the flexibility to adjust reproductive activity to variable environmental conditions each year. Future work should elucidate whether food provides nutritional or non-nutritional cues, and the neurophysiological mechanisms by which food stimulates reproductive activity.     

Phenotypic plasticity of reproductive traits in response to food availability and photoperiod in white-footed mice (Peromyscus leucopus)

Changes in photoperiod, ambient temperature and food availability trigger seasonal acclimatization in physiology and behavior of many animals. In the present study, seasonal adjustments in body mass and in several physiological, hormonal, and biochemical markers were examined in wild-captured plateau pikas (Ochotona curzoniae) from the Qinghai-Tibetan plateau. Our results showed that plateau pikas maintained a relatively constant body mass throughout the year and showed no seasonal changes in body fat mass and circulating levels of serum leptin. However, nonshivering thermogenesis, cytochrome c oxidase activity, and mitochondrial uncoupling protein 1 (UCP1) contents in brown adipose tissues were significantly enhanced in winter. Further, serum leptin levels were positively correlated with body mass and body fat mass while negatively correlated with UCP1 contents. Together, these data suggest that plateau pikas mainly depend on increasing thermogenic capacities, rather than decreasing body mass, to cope with cold, and leptin may play a potential role in their thermogenesis and body mass regulation.     

Photoperiodic polyphenisms in rodents: neuroendocrine mechanisms, costs, and functions

Annual changes in daylength figure prominently in the generation of seasonal rhythms in reproduction, and a wide variety of mammals use ambient photoperiod as a proximate cue to time critical reproductive events. Nevertheless, within many reproductively photoperiodic mammalian species, there exist individuals--termed "photoperiod nonresponders"--that fail to adopt a seasonal breeding strategy and instead exhibit reproductive competence at a time of year when their conspecifics are reproductively quiescent. Photoperiod nonresponsiveness has been principally characterized by laboratory observations--over half of the species known to be reproductively photoperiodic contain a proportion of nonresponsive individuals. The study of nonresponders has generated basic insights regarding photic regulation of reproduction in mammals. The neuroendocrine mechanisms by which the short-day photoperiodic signal is degraded or lost in nonresponders varies between species: differences in features of the circadian pacemaker, which provides photoperiodic input to the reproductive neuroendocrine system, have been identified in hamsters; changes in the responsiveness of hypothalamic gonadotrophs to melatonin and as-yet-unspecified inhibitory signals have been implicated in voles and mice. Individuals that continue to breed when their conspecifics refrain might enjoy higher fitness under certain circumstances. Statements regarding the adaptive function of reproductive nonresponsiveness to photoperiod require additional information on the costs (metabolic and fitness) of sustaining reproductive function during the winter months and how these costs vary as a function of environmental conditions. Reproductive nonresponders thus continue to represent a challenge to theories that extol the adaptive function of seasonality. Several nonexclusive hypotheses are proposed to account for the maintenance of nonresponsive individuals in wild rodent populations.     

Photoperiod and food restriction differentially affect reproductive and immune responses in Siberian hamsters Phodopus sungorus

1.  Organisms must contend with seasonal fluctuations in energy availability. To maintain a positive energy balance year-round, a number of adaptations have evolved including seasonal changes in reproduction, energetics and immunity. Photoperiod is the primary environmental signal most animals use to predict seasonal events. Despite the established link between energetics and immune function, little is known regarding how changes in energy availability affect immunity.
2.  The goal of the present study was to determine the effects of food restriction on photoperiodic changes in reproduction and immune function in the Siberian hamster ( Phodopus sungorus ). Adult hamsters were housed in long or short days and were food restricted or fed ad libitum . Immune responses were quantified by measuring specific antibody production and bacterial killing capacity.
3.  Food restriction decreased body and relative reproductive masses in long-day animals. Antibody responses, but not bacterial killing ability, were enhanced in food restricted short-day animals as compared with ad libitum fed controls. We also found differential effects of body fat on immune responses depending on the immune measure.
4.  The effects of food restriction on immune function appear to vary based on the restriction regimen, the response measured, and the physiological state of the organism including energy balance, metabolic rate and reproductive status.
5.  In conclusion, these results suggest that a wide range of factors can differentially affect immune function. In addition, these effects may vary based on the specific response examined. Future studies should include a variety of measurements to provide a more integrative and accurate picture of reproductive, energetic, and photoperiodic effects on immune function.     

Seasonal pre‐migratory fattening and increased activity in a nomadic and irruptive migrant,the Red Crossbill Loxia curvirostra

It is well documented that irruptive and nomadic migrants move in response to resources that are distributed unpredictably in space, time or both. Increasing evidence, however, suggests that irruptive and nomadic species may use seasonal timing mechanisms to prepare for migrations, despite the more facultative nature of their movements. Here we use data from free‐living and captive Red Crossbills Loxia curvirostra, a typical irruptive nomad, to examine three hypotheses regarding control of facultative migration: (1) the facultative migration hypothesis, which states that both preparation and departure decisions are regulated by resource availability; (2) the seasonal preparation hypothesis, which states that preparation is initiated by seasonal factors (i.e. endogenous rhythms and/or photoperiod) but that departure decisions are dependent on local resource availability; and (3) the seasonal migration hypothesis, which states that both preparation and departure decisions are initiated by seasonal mechanisms and are independent of local food resources. Red Crossbills in North America are thought to make temporally consistent spring migrations in anticipation of conifer cone maturation. In this study, fat deposits of free‐living Red Crossbills peaked in May and June, exceeding even winter deposits. In agreement with the field data, captive birds on a natural photoperiod with constant food and temperature showed a peak in fat deposition and activity levels in June. These findings are consistent with the seasonal preparation and the seasonal migration hypotheses and contribute to a growing literature that suggests that facultative migrants may prepare for movements in similar ways to seasonal migrants.     

白头鹎肝脏和肌肉冬夏两季的代谢产热特征比较

动物能量代谢的生理生态特征与物种的分布和丰富度密切相关,基础代谢率(basal metabolic rate,BMR)是恒温动物维持正常生理机能的最小产热速率,是内温动物能量预算的重要组成部分.该文以白头鹎(Pycnonotus sinensis)为研究对象,分别在冬季和夏季测定了白头鹎的体重、BMR、肝脏和肌肉的线粒体蛋白质含量、线粒体呼吸及细胞色素C氧化酶(cytochrome c oxidase,COX)活力及血清中甲状腺素(T4)及三碘甲腺原氨酸(T3)含量的变化,从细胞和酶学水平上解释白头鹎基础产热的季节适应规律.耗氧量采用封闭式流体压力呼吸测定仪测定,肝脏和肌肉的线粒体状态4呼吸及COX活力采用铂氧电极-溶氧仪测定.结果显示:白头鹎的体重和BMR冬季显著高于夏季;肝脏和肌肉的线粒体呼吸,以及肝脏和肌肉的COX活力冬季明显高于夏季;血清T3浓度冬季较高,夏季较低.这些结果表明:在野外自然条件下,肝脏和肌肉在细胞水平产热能力的提高和血清T3含量的增加是白头鸭BMR增加的细胞学机制之一,同时是白头鹎抵御冬季寒冷的一种重要方式.